<%BANNER%>

Natural Licks as Keystone Resources for Wildlife and People in Amazonia

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NATURAL LICKS AS KEYSTONE RESO URCES FOR WILDLIFE AND PEOPLE IN AMAZONIA By OLGA LUCIA MONTENEGRO A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLOR IDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY UNIVERSITY OF FLORIDA 2004

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Copyright 2004 by Olga Luca Montenegro

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This dissertation is dedicated to the memory of my father, Jos J. Montenegro, from whom I inherited his curiosity for animals, his love for nature and his spirit of adventure; to my mother Blanca Lilia who, together with my father, gave me all the values that guide my life; to my brothers Alvaro and Gabriel, and my sisters Marlene and Doris and their beautiful families, whose love and support are with me always; and. to Don, whose love, friendship and encouragement help me to pursue my dreams.

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iv ACKNOWLEDGMENTS I would like to star t by thanking my supervisory co mmittee chair and co-chair, Dr. Richard Bodmer and Dr. George Tanner. Dr. Bodmer provided valuable academic advice during the whole process of co mpleting my studies, and critic al support for my fieldwork in the Peruvian Amazon. Dr. Tanner helped me with valuable comments on my work and important suggestions for my analyses a nd writing. Also, the other members of my academic committee, Dr. Melvin Sunquist, Dr. Lyn Branch and Dr. Lee McDowell provided significant suggestions and support during several stages of this study, and critical review of previous versions of this document. A former member of my supervisory committee, Dr John Eisenberg (deceased) provided im portant suggestions and encouragement in the early stage of this study. Although he is not with us anymore, his deep knowledge and his teachings have been of great value on our understanding of tropical mammal ecology. Many other people contributed in differe nt ways to this study. Donald Mee patiently reviewed several ve rsions of this document, and helped me to improve it significantly. His critical comme nts, philosophical discussions, and constant support have been very important for me all these years. Pablo Puertas, Miguel Antnez, and Kati Salovaara provided support and companionship during the fieldwork. Also cr ewmembers of the research vessel Nutria, Julio Curinuqui, Gilberto Asipali, Fredy Curi nuqui and Jorge Pacaya, and field assistants Tedy Alvarado, Juan Huanaquiri, Jos Ariram a, Pablo Asipali and Oliver Rodrguez

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v helped during our work in the Yavari-Mir i River. During year 2002, Colombian master student Carolina Lozano joined the expedition and helped in many ways with the fieldwork. During the same year also, Jairo Huanaquiri of Village Esperanza, provided very important help, going with us along th e Esperanza Creek and Yavari-Miri River, mapping and measuring natural licks. His sens e of humor and knowledge of the area and the animals made of the fieldtri p a fun and productive experience. Community members of Villages Esperanza, San Felipe and Carolina, on the Yavari-Miri River kindly received us in their homes and shared with us their experiences, knowledge and friendship. They al so shared with us their masato (a fermented drink), soccer games, and parties, making us feel welcome and at home. In Iquitos, Roberto Pezo, dean of Biologi cal Sciences Department of Universidad Nacional de la Amazonia Peruana, provided institutional support. Also, Nancy Arvalo, former director of Herbarium Amazonence, kind ly let us reviewing our plant material at the herbarium, and botanist Juan Ruiz provided important help with plant identification. In Colombia, Hugo Lpez, assistant pr ofessor at Universidad Nacional de Colombia greatly contributed in several form s to this study, both in Leticia and Bogot, with critical suggestions, and in kind suppor t and friendship. Also, Gonzalo Andrade, director of Instituto de Ciencias Natura les provided institutional support. Professor German Palacio, director of Instituto Imani, at Universidad Naci onal de Colombia at Leticia, also helped with some of the logistic s. Also at Leticia, Juan Echeverri, Martha Pabn, Pablo Palacios, Carlos Za rate and Edwin Agudelo gave support in the early stages of the fieldwork. Fundacin Terrapreta, in Bogot assisted with the soil analyses, and soil scientist Pedro Botero, helped with the interpretation of results. Corporacin

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vi Colombiana de Investigacin Agropcuaria CORPOICA, helped with plant and tapir fecal mineral analyses. Also, in Colombia many colleagues and fr iends helped me on different occasions. Dr. Alberto Cadena, former curator of the ma mmal laboratory of the Museum of Natural History at Universidad Naciona l de Colombia was my first mammal professor and greatly inspired my interest in this group of animals. He always encouraged us to keep studying and increasing our understanding of our wild an imals. Pedro Sanchez, assistant professor of Biology gave me encouragement and valu able friendship. Marcel a Gomez, Francisco Snchez, Alba Lucia Morales, and Manuel Paez helped me to prepare some of the materials for the fieldwork. Juliana Rodriguez helped me on several occasions in processing part of my samples. Aida Otlora, Silvia Alvar ez, and Elizabeth Meza helped in entering or reviewing some of my data files. Patricia Medici, chair of the Tapir Specialist Group (TSG) of IUCN, Diego Lizcano and other members of TSG shared with me their knowledge on tapirs and provided several opportunities to present and discuss preliminary results of this study. My friend Ge rman de la Hoz taught me many things and I will always be grateful for his support. In Gainesville, many people helped me in several ways to successfully complete this study and my academic work at the Universi ty of Florida. Dr. Nat Frazer, chair of the Department of Wildlife Ecology and Conserva tion provided essential support at the department. Faculty and staff were also very helpful in all stages of this process and always provided me rapid and efficient so lution to any difficulty, when needed. My friends at University of Florida, Maria Ines Barreto, Carlos Jaramillo and Cristina Dockx helped me with handling part of my field e quipment and ensured that it reached me in the

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vii field. Also, other friends at UF Marcela Machicote, Sonia Ca navelli, Ivan Diaz, Santiago Espinosa, Alejandro Paredes, Luis Ra mos and Margo Stoddard listened to my monologues about my research and provide me with great suggestions. Matthew Bokach patiently oriented me with ArcView. My officemates and friends Christine Lucas, Ian Fiske, Matthew Trager, Chantavy Vongkhamh eng, and Maynard Hiss also provided good insights and great companion. Martha Castaeda, Victoria Mejia, Diana (Tita) Alvira, Mutsuo Nakamura and other friends also made of my live in Gainesville a very enjoyable experience. James Albury from the Center for Instructional and Research Computing Activities (CIRCA) at University of Florid a helped me in the final formatting and electronic submission of this dissertation. Several institutions provided funding for this study. The Tropical Conservation and Development Program of the Center for Latin American Studies at University of Florida provided a preliminary fieldwork travel gran t. Idea Wild supported my work by donating 3 camera traps. The Columbus Zoological Park Association provided two research awards in 2001 and 2002 for partial funding of some components of this study, including equipment and expenses related to laborator y analyses. Wildlife Conservation Society provided financial support to the research and conservation program coordinated by Dr. Richard Bodmer, within which this study wa s conducted. Collection and research permits were issued by the Institute of Na tural Resources, INRENA, in Per. My studies at the University of Flor ida were supported by several sources. Fulbright Commission and LA SPAU provided me a fellowshi p for my master program. The Tropical Conservation and Development Pr ogram of the Center for Latin American Studies, the Department of Wildlife Ecology and Conservation and the Florida Museum

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viii of Natural History provided me on different occasions with res earch, extension and teaching assistantships that allowed me to pursue a Ph. D. degree. In Colombia, COLFUTURO provided important financial support during the last year of my studies at University of Florida. Finally, my family has always supported me in all my decisions and has given me its love and support. This re search and my studies at the University of Florida would not have been possible without the support from all the above people and institutions, and I am deeply grateful to all of them.

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ix TABLE OF CONTENTS page ACKNOWLEDGMENTS.................................................................................................iv LIST OF TABLES............................................................................................................xii LIST OF FIGURES.........................................................................................................xiv ABSTRACT.....................................................................................................................xv i CHAPTER 1 INTRODUCTION........................................................................................................1 2 NATURAL LICK USE BY AMAZONI AN WILDLIFE IN NORTHERN PERU.....7 Introduction................................................................................................................... 7 Study Area....................................................................................................................9 Methods......................................................................................................................11 Camera Trapping.................................................................................................12 Direct Observation...............................................................................................12 Examining Tracks................................................................................................13 Data Analyses......................................................................................................13 Lick visitors..................................................................................................13 Frequency of natural-lick use.......................................................................13 Lick-visitation rate a nd species abundance..................................................15 Results........................................................................................................................ .15 Lick Visitors........................................................................................................15 Frequency of Natural-Lick Use...........................................................................16 Camera traps.................................................................................................16 Direct observation........................................................................................17 Examining tracks..........................................................................................18 Variation in Lick Use through the Year..............................................................18 Lick-Visitation Rates and Species Abundance....................................................18 Discussion...................................................................................................................19 Lick Visitors........................................................................................................19 Frequency of Lick Use........................................................................................23 Lick-Visitation Rate a nd Species Abundance.....................................................25 Summary and Conclusions.........................................................................................25

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x 3 NATURAL LICK SOILS AS SOURCE OF MINERALS FOR WILDLIFE IN THE YAVARI-MIRI REGION..........................................................................................34 Introduction.................................................................................................................34 Study Site....................................................................................................................3 7 Methods......................................................................................................................39 Lick Location and Description............................................................................39 Physical and Chemical Char acterization of Lick Soils.......................................39 Soil sampling................................................................................................39 Laboratory analyses......................................................................................40 Data analysis................................................................................................41 Results........................................................................................................................ .41 Lick Location and Description............................................................................41 Physical and Chemical Char acterization of Lick-Soils.......................................43 Particle size..................................................................................................43 Chemical properties of lick and nonlick soils............................................43 Discussion...................................................................................................................45 Lick Location and Description............................................................................45 Physical and Chemical Ch aracterization of Licks...............................................47 Particle size..................................................................................................47 Chemical properties of lick and nonlick soils............................................48 Summary and Conclusions.........................................................................................52 4 BROWSE AND FRUIT AS A SOURCE OF MINERALS FOR LOWLAND TAPIR IN THE YAVARI-MIRI REGION................................................................58 Introduction.................................................................................................................58 Study Area..................................................................................................................62 Methods......................................................................................................................62 Lowland Tapir Diet in the Yavari-Miri Region..................................................62 Determination of Minerals in Tapir Food and Fecal Samples............................64 Data Analyses......................................................................................................65 Results........................................................................................................................ .66 Lowland Tapir Diet at the Yavari-Miri Region...................................................66 Minerals in Lowland Tapir Food.........................................................................67 Discussion...................................................................................................................70 Lowland Tapir Diet at the Yavari-Miri Region...................................................70 Minerals in Lowland Tapir Food.........................................................................72 Summary and Conclusions.........................................................................................76 5 NATURAL LICKS AND RURA L PEOPLE OF THE AMAZON...........................86 Introduction.................................................................................................................86 Study Area..................................................................................................................88 Location and Biophysical Setting........................................................................88 History and Description of Nueva Esperanza Village.........................................88 Methods......................................................................................................................91

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xi Subsistence Hunting Records..............................................................................91 Natural Lick Mapping and Description...............................................................92 Hunters Perceptions Concerning Natural Licks.................................................92 Results........................................................................................................................ .93 Subsistence Hunting in Nueva Esperanza Village..............................................93 Natural Lick Mapping and Description...............................................................94 Hunters Perceptions Concerning Natural Licks.................................................95 Discussion...................................................................................................................96 Subsistence Hunting Records..............................................................................96 Natural Lick Mapping and Description...............................................................98 Hunters Perceptions Concerning Natural Licks.................................................99 Summary and Conclusions.......................................................................................101 6 SYNTHESIS AND CONCLUSIONS......................................................................110 LIST OF REFERENCES.................................................................................................116 BIOGRAPHICAL SKETCH...........................................................................................128

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xii LIST OF TABLES Table page 2-1 Sampling effort used in three detecti on methods to determine the frequency of natural-lick use by wildlife in the Ya vari-Miri River Vall ey, during year 2001......26 2-2 Sampling effort used in direct observation per season.............................................26 2-3 Species detected at natural licks by ca mera trapping, direct observations and tracks in the Yavari-Miri Rive r valley, Peruvian Amazon.......................................27 2-4 Number of monthly phot o-captures at 14 licks form March to December 2001, in the Yavari-Miri River Valley, Peruvian Amazon................................................28 2-5 Frequency of birds and mammals observed at eight natural licks from February to early December (excluding August), 2001 in the Yavari-Mirin River Valley, Peruvian Amazon.....................................................................................................29 2-6 Chi-square values for testing the null hypothesis that number of sightings is the same in the three seasons.........................................................................................30 3-1 Number of soil samples from lick and nonlick sites gathered in year 2001 in the Yavari-Miri River valley in the Peruvian Amazon..................................................53 3-2 Descriptive features of 24 natural li cks in the upper Yavari-Miri River valley, Peruvian Amazon.....................................................................................................54 3-3 Chemical characterization of soils from lick and non-li ck sites in two seasons of year 2001 in the Yavari-Miri River valley in the Peruvian Amazon.......................55 3-4 Microminerals in lick and non-lick so ils during the high water season of 2001, in the Yavari-Miri River valle y in the Peruvian Amazon........................................56 4-1 Plant species in tapir browse along th e Yavari-Miri River, Peruvian Amazon.......78 4-2 Number of composite samples of each family analyzed for mineral concentrations in 2 seasons in the Yava ri-Miri River valley, Peruvian Amazon....80 4-3 Fruits in lowland tapir diet in the Yavari-Miri River vall ey, northeastern Peruvian Amazon.....................................................................................................81

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xiii 4. 4 Mean content of nitrogen and macrominer als in tapir foods (browse and fruits), suggested requirements (based on gui delines for horses) and mean concentrations of excreted N a nd macrominerals in tapir feces...............................82 4-5 Mean content of microminerals in ta pir foods (browse and fruits), suggested requirement (based on guidelines for hor ses) and mean concentrations of excreted microminerals in tapir feces.......................................................................83 5-1 Species hunted by settlers of Nueva Es peranza Village in the Yavari-Miri River from January to December 2001............................................................................103

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xiv LIST OF FIGURES Figure page 2-1 Location of 24 natural licks found in the Yavari-Miri RiverValley, northeastern Peru......................................................................................................30 2-2 Photo-captures per 100 tr ap-night per species at 14 licks from March to December 2001 in the Yavari-Mirin Rive r Valley, Peruvian Amazon (excludes bats).......................................................................................................................... 31 2-3 Total sighting rate of bird species at 8 licks surveyed from February to early December 2001 in the Yavari-Miri River Valley, Peru...........................................31 2-4 Total sighting rate of diurnal mammal sp ecies at 8 licks surveyed from February to early December 2001 in the Yavari-Miri Valley, Peru........................................32 2-5 Total sighting rate of nocturnal mamm al species at 8 licks surveyed from February to early December 2001 in the Yavari-Miri Valley, Peru.........................32 2-6 Ratio of track occurrences for tapir ( Tapirus terrestris ), white-lipped peccary ( Tayassu pecari ), collared peccary ( Pecari tajacu ), and red-brocket deer ( Mazama americana )...............................................................................................33 2-7 Density of selected mammals in the Ya vari-Miri River valley and their overall lick-visitation rate during year 2001........................................................................33 3-1 Location of the study site in the Yavari -Miri River valley, in northern Peruvian Amazon....................................................................................................................56 3-2. Mean content of sand, silt and clay in samples from lick and non-lick soils. Size of vertical lines indicates 1 standard deviation.....................................................57 4-1 Percent distribution of plant families browsed by lowland tapir ( Tapirus terrestris ) in the Yavari-Miri River valley, of the northeastern Peruvian Amazon.....................................................................................................84 4-2 Percentage of occurrence of several fr uit species in lowland tapir feces along the Yavari-Miri River valley, Peruvian Amazon...........................................................84 4-3 Concentration of macrominerals in tapi r browse, during high water and low water seasons in the Yavari-Miri Rivi er valley, Peruvian Amazon...................................85

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xv 4-4 Concentration of trace minerals in ta pir browse during high water and low water seasons in the Yavari-Miri Ri ver valley, Peruvian Amazon....................................85 5-1 Location of the study area in the Ya vari-Miri River region, northeastern Peruvian Amazon...................................................................................................105 5-2 Gender and age composition of Nueva Es peranza Village in the Yavari-Miri River region, northeastern Peruvian Amazon (census conducted in 2002)...........106 5-3 Percent contribution of each species to the total number of animals hunted in 2001 in the Yavari-Miri River................................................................................106 5-4 Percent contribution of each species to the total biomass hunted in 2001 in the Yavari-Miri River...................................................................................................107 5-5 Proportion of biomass harvested by hunters of the Nueva Esperanza Village per hunting site from January to December 2001........................................................108 5-6 Biomass hunted per ungulate species at riverbanks, natural licks and hunting trails in the Yavari-Miri Ri ver region during year 2001........................................108 5-7 Location of hunting areas and natural licks used by settlers of Nueva Esperanza village.....................................................................................................................109

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xvi Abstract of Dissertation Pres ented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy NATURAL LICKS AS KEYSTONE RESO URCES FOR WILDLIFE AND PEOPLE IN AMAZONIA By Olga Lucia Montenegro December 2004 Chair: Richard E. Bodmer Cochair: George Tanner Major Department: Wildlife Ecology and Conservation Natural licks are particular sites in some types of habitats often visited by a number of wild animals with the pur pose of licking or consuming soil (a behavior known as geophagy). Several studies asso ciate geophagy with the nutriti onal ecology and/or health of the animals that use them. Therefore, the existence of natural licks in a particular habitat may reduce the costs of obtaining ade quate nutrition, and/or maintaining health; and thus may be fundamental to population pers istence. One of the habitats where natural licks exist is the Amazon forest. Many Amaz onian wildlife species, including large birds and herbivorous mammals, are users of natural licks. Natural licks also may be important for rural communities that rely on wildlife for their subsistence. This is particularly important for Amazonian human communities, because one of the most common hunting techniques in those forests is waiti ng for game animals at natural licks.

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xvii Our study addressed the importance of natura l licks for both wild life and humans in the Yavari-Miri River valley in the northeas tern Peruvian Amazon. A relatively large group of mammalian and large bird species fre quently visited natural licks during 2001. The most frequent lick visitors were lowl and tapirs. Natural licks found in the YavariMiri River valley had higher concentration of se veral minerals (Na, Ca, Mg, P, Cu, S, and B) compared to non-lick samples. Those diffe rences were constant throughout the year; suggesting that natural licks ar e in fact, a source of minerals for wildlife in the YavariMiri River valley. The diet of the most-fre quent lick visitor (the lowland tapir) was examined for mineral content. Results show ed that combined foods eaten by lowland tapirs are of good quality rega rding mineral content, except for Na, P, Cu and Zn. We suggest that tapirs supplemen t their mineral intake by consuming mineral-rich soils at natural licks in the Yavari-Mir i River valley. The above result s suggest that natural licks are a key resources for several Amazonian species because they represent a natural mineral source in the humid fo rest of western Amazonia. To assess the importance of natural li cks for Amazonian human communities, subsistence-hunting patterns were examined at the Nueva Esperanza village, in the Yavari-Miri River valley. Ov er 30% of total biomass hunt ed during 2001 was harvested at licks, and was heavily represented by lo wland tapirs. Hunters of Nueva Esperanza village use more than 40 natural licks lo cated along the Esperanza Creek and the middle and lower Yavari-Miri River. We recommend regulation of hunting at licks by temporal rotation of use. Also, we suggest that natural licks should be an attrib ute of habitat quality when selecting areas for wildlife conservation in western Amazonia.

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1 CHAPTER 1 INTRODUCTION In wildlife ecology, a resource has been simply described as something an animal needs (Caughley & Sinclair 1994:46). The conservation biology discipline has introduced the term keystone resources to refe r to those resources th at are critical or limiting in particular habitats, but are crucia l for many species in a community (Primack 1993). The above concept is an extension of th e keystone term used in other contexts. The term keystone was first used in ecology to refer to a predator species of exceptional importance because of its critical effect on prey populations in main taining the structure of its community (Paine 1969). Since then, th e concept of a keyst one species has been extended to many species across trophic levels and has been catego rized according to their function and community importance (key stone predator, prey, mutualist, host, modifier; Mills et al 1993). Power et al (1996:609) proposed a refined definition for the keystone as a species whose impact on its community or ecosystem is large, and disproportionately large relativ e to its abundance. The keystone role has been extended not only to species (both plants and animals), but also to cr itical limiting resources that occupy only a small area of the habitat, a nd yet are critical to many species in the community (Primack 1993:48). Natural licks are listed among those keys tone resources (Primack 1993). Natural licks are particular sites in some types of habitats often visited by a number of wild animals with the purpose of licking or c onsuming soil. This behavior, known as geophagy, is common among many mammals (ungulat es, primates, rodents) and several

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2 species of birds. Geophagy has been reporte d in many geographical locations throughout the world. Because ingested soils usually have a hi gh content of one or several minerals and/or a higher clay content compared to non-eaten soils, several benefits of geophagy have been proposed. One hypothesis is that mi nerals in lick soil compensate for mineral deficiencies or imbalances (Jones & Hanson 1985). This is why researchers usually refer to geophagy sites as mineral licks or salt lic ks. Another hypothesis is that the clay in eaten soil has beneficial effects on decr easing acidosis, secondary plant compounds, intestinal infections or pa rasites (Mahaney 1993; Mahaney et al 1996, 1997; Gilardi et al 1999). Those studies refer to the licks as clay licks. These hypotheses may not be mutually exclus ive. Comparing data across studies is difficult because of the different research questions and methods used in each case (reviews in Kreulen 1985; Klaus & Schmid 1998; Diamond et al 1999; Krishnamani & Mahaney 2000). The overall conclusion of t hose reviews is that geophagy has different functions for different animal species, and/or different functions for the same species under different situations. However, all propos ed reasons for soil consumption at natural licks (as are called hereafter) seem related to the nutritional ecology a nd/or health of the animals that use them. Therefore, the existence of natural licks in a particular habitat may reduce the costs of obtaining adequate nutriti on, and/or maintaining health; and thus may be fundamental to population persistence. One of the habitats where natural licks ex ist is the Amazon forest, particularly in western Amazonia. Many wildlife species (m ainly ungulates, primates, and rodents, and some birds species) are users of natural lick s. Preliminary research in the Peruvian

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3 Amazon indicated that during the dry season in the southern Peruvian Amazon, lowland tapirs and other ungulates are frequent li ck users (Montenegro 1998). However, it is poorly known whether the use of licks is cons tant through the year, or occurs mainly during dryer seasons. Also, in that pilot study, further research on dietary mineral contents of lowland tapir food was suggest ed to better examine the mineral-intake hypothesis for tapirs in the Amazon forest. Natural licks also may be important for rural communities that rely on wildlife for their subsistence. For many Amazonian rura l communities, wildlife hunting continues to be one of the most important subsis tence sources (Robinson & Bodmer 1999). A potential keystone role of natural licks for local hunters could be hypothesized, since one of the most common hunting techniques in the Amazon forest is waiting for game animals at natural licks. At the Tamshiy acu-Tahuayo Communal Reserve (RCTT) in the Peruvian Amazon, the presence of natural licks, known as colpas is often an indispensable condition for establishing hun ting sites (Puertas 1999). One important hunting strategy used by local hunte rs at the RCTT is going to the colpas at night looking for tapirs, deer and pacas (Puertas 19 99). Moreover, Puertas (1999) provided one example of a hunter strate gically placing food in colpas to accustom animals to supplied fruits. This practice allowed the hunter to rotate hunting sites over time. Although the use of natu ral licks as hunting sites is commonly reported, few studies have quantified the relative importance of thos e places in terms of the amount of game obtained in relation to total hunting. The few published studies on this subject involve use of licks by native groups. In the Colo mbian Amazon, for example, indigenous communities of the Miriti-Parana River obtain about 25% of consumed meat from natural

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4 licks (Walshburger & Hildebrand 1988). No ot her estimations of hunting return from natural licks are published, and the real importa nce of licks as hunting sites is generally poorly known in Amazonian hunting systems. Over-hunting at natural licks was appare ntly controlled by social and ritual practices in many indigenous communities. For many Amazonian communities, however, such restrictions are no longer practiced, or ar e not part of their culture, especially for settlers who migrated from other regions. As a result, hunting at natu ral licks is usually uncontrolled. Often hunters report that a natural lick has been damaged when animals, as a consequence of excessive hunting, no longer visit it. Intensive hunting at natural licks drives animals away, probably affecting their nutrition and health. Over-explo itation of many wildlife specie s also is contributing to declines in their populations. This is particularly true for ungul ates such as lowland tapirs and large primates (Bodmer et al .1993, 1997b). At the same time, over-exploitation of wildlife at natural licks may threaten subsistence of rural communities that depend on wildlife as their main source of subsistence. For the above reasons, a better understanding of the importance of natural licks as a re source for Amazonian wildlife, and for rural communities in the Amazon is needed in order to design effective wildlife-management programs that take into account both rural communities subsistence and long-term wildlife persistence. From the above background, these questions arise: how importan t are natural licks for both wildlife and people in western Amazonia? Can they be considered as a keystone resource in that habitat? Peres (2000) proposed that 4 eco logical attributes could be examined in order to help identifying putative keystone resources: (1) degree of

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5 consumer specificity, (2) temporal redundancy, (3) reliability, and (4 ) abundance. From the consumers perspective, a keystone resource is one with low redundancy (available when alternative sources are not), is cons umed by a large pro portion of the species assemblage, is highly reliable, and has low abundance. Although Peres (2000) proposed these attributes to identify putative keystone plant resources, they appear useful to examine the potential keystone role of other resources. For this reason, the above attributes are us ed here as a framework to examine the importance of natural licks in western Amazoni a. If natural licks can be considered a keystone resource for both wildlife and people in western Amazonia, the following results would be expected: (1) a high number of lick users (both wildlife and people) visit the licks, (2) natural licks provi de something to their users th at is in short supply and is not easily substitutable (low redundancy), (3) natural licks are a reliable resource (are available when users need them), and (4) area occupied by natural licks in the habitat is small relative to its effect on its users. Our study addressed the importance of natura l licks for both wild life and humans in a site of western Amazonia, the Yavari-Miri River valley of northeastern Peru. The study is presented in 4 components addressing the following objectives: Objective 1 : To identify the wildlife species that are the most frequent licks users, to describe their pattern of visitation through the year, a nd to examine whether they visit licks in proportion to their abundance in the Yava ri-Miri River valley in northeastern Peruvian Amazon. Objective 2: To evaluate natural licks as a source of minerals for Amazonian herbivores, and to describe the licks in terms of their size and location in the Yavari-Miri River valley. Objective 3 : To examine the mineral intake hypothesis for lowland tapirs by determining the mineral content of tapir food a nd tapir feces.

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6 Objective 4 : To examine the importance of natu ral licks for subsistence hunting in an Amazonian rural community, and its implications for management and conservation. The following hypotheses were tested: Hypothesis 1 : A relatively large number of species use licks, at least during part of the year. Hypothesis 2 : For at least for some species, their use of natural licks is higher than expected from their abundance in the area. Hypothesis 3 : Soils at natural licks have higher mineral concentrations (at least for one or more minerals) than non-lick soils. Hypothesis 4 : Lowland tapir food is limited in one or more mineral nutrients in the Yavari-Miri River valley and such lim itation is constant through the year. Hypothesis 5 : Excretion of limited minerals (at least for some minerals) is low in tapir feces. Hypothesis 6 : Hunting at natural licks provides a higher contribution to the overall harvest, at least for some species, as compared to other hunting sites. Hypothesis 7 : Most rural hunters in a community of western Amazonia use natural licks as hunting sites Chapter 2 addresses hypotheses 1 and 2, ex amining the pattern of natural lick use by Amazonian wildlife in the Yavari-Mir i River region. Chapte r 3 deals with the properties of consumed soils at natural licks, to examine hypothesis 3. Chapter 4 discusses browse and fruit as sources of minerals for lowl and tapir, and mineral fecal excretion, to address hypotheses 4 and 5. Chap ter 5 describes the use on natural licks by a rural community in the Yavari-Miri Rive r, addressing hypotheses 6 and 7. Finally, Chapter 6 presents a synthesis of results and its implications for wildlife conservation in the Yavari-Miri River valley.

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7 CHAPTER 2 NATURAL LICK USE BY AMAZONIAN WILDLIFE IN NORTHERN PERU Introduction Wildlife species around the world use natu ral licks. Many of those species are either mammals (Klaus & Schmid 1998; Krishanmani & Mahaney 2000) or birds (Diamond et al. 1999; Gilardi et al. 1999). Among mammals, ungul ates visit natural licks in diverse habitat types. Muskox and caribou in tundra (Calef & Lo rtie 1975; Klein & Thing 1989), moose in boreal forests (Frase r & Hristieko 1981;Tankersley & Gasaway 1983; Couturier & Barrete 1987; Miller & Livitatis 1992), and white-tailed deer in many locations in North America (Weeks & Kirkpatrick 1976, Atwood & Weeks 2002) are some examples of ungulates using licks in temperate regions. For tropical areas, information on lick use exists mainly for areas of the Old World. African elephants (Holdo et al 2002) and seven other ungulate spec ies in savannas and woodlands (Henshaw & Ayeni 1971), Asian elephant and other ungulates in tr opical forest of Thailand, and babirusa in Indonesia (Cla yton & MacDonald 1999) are some large mammals using natural licks in the tropics. Besides ungulates, more than ten species of Old World primates are reported to eat soil from licks or th e forest floor (Krishmamani & Mahaney 2000). Much less is known about na tural lick use in the Neotropics. Few publications exist, other than occasional reports of primates using licks (Heymann & Hartmann 1991; Izawa 1993; Ferrari 1995; Mller et al 1997), tapir observations at a few sites (Pea et

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8 al 1996, Montenegro 1998, Lizcano & Cavelier 2000), and a study on the physiological significance of geophagy for some species of birds (Gilardi et al 1999). In both temperate and tropical regions, re search dealing with natural lick use has addressed soil consumption (or geophagy), and its physiological significance to the animals. Several non-exclusive hypotheses transcend geographic ar eas and/or species (Kreulen 1985; Klaus & Schmid 1998; Diamond et al 1999; Krishnamani & Mahaney 2000). The overall view is that soil consum ption at natural licks is linked to the nutritional ecology (Chapter 4) a nd/or health of the lick users. Besides the benefits for the animals nutrition and/or health, licks may also function as animal-gathering places, facilitating social encounters (Coutur ier & Barrete 1987, Ruggiero & Fay 1994). Since natural licks may have more than one function for wildlife species, and those functions may vary across species, licks may represent a resource whose ecological importance goes beyond the particular benefits for individual species. As suggested by Klaus & Schmid (1998), presence of natural lick s in some habitats may have an effect on population densities and structur e, and may influence the carr ying capacity of areas with lick sites. Studies ra rely discuss natural lick use at a community-wide level with a broader ecological perspective. The ecological importance of natural licks could thus be overlooked. We need to know which species in a give n region use licks, how often they use them, and whether that use differs among speci es to assess the significance of licks as a resource for wildlife in that region. In the Amazon rainforest, this knowledge is limited, but it may have ecological and conservation implications.

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9 This chapter examines the use of natura l licks by wildlife species in the YavariMiri River valley in the nor theastern Peruvian Amazon. Th e following questions were addressed: Question 1 .Which species use natural licks in the Yavari-Miri River valley? Question 2 .Do all species use licks with th e same frequency, and does that frequency vary through the year? Question 3 Do the species use licks in proportion to their abundance in the area? These questions were addressed by invent orying all lick visitors, by comparing lick visitation rates among species th roughout the year, and by rela ting lick-visitation rates to available data on species abundance. If natu ral licks are a resour ce of community-wide importance in the Amazon forest, it is expected that a variety of speci es use licks, at least during part of the year, and that at least for some species, their use of the licks is higher than expected from their abundance in the area. Study Area The study area was located along the Yavar-M ir River, a tributary of the Yavar River (Yavari District), Mariscal Ramn Ca stilla Province, Department of Loreto, in northeastern Peru. Fieldwork was conducted th roughout the middle course of the YavariMir River, in the area between 4o30.23S, 72o26.69W and 4o24.77S, 72o09.76W (Figure 2-1). Weather stations on this river do not exist, but the areas climate conditions were approximated from the closest stati ons in and around Iquito s (Marengo 1998), about 170 km northwest of the middle course of the Yavari-Miri River. The region is warm and humid. Mean annual temperature is 26oC, with monthly mean maximum temperatures ranging from 28 to 30oC, and monthly mean minimum temperatures from 17 to 20oC. Temperature drops below the minimu m average for 3 to 5 days during friagem an event

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10 occurring between May and September, in which cold dry air masses coming from the South Pole arrive in the Amazon basin (Marengo 1984). Mean annual precipitation ranges from 2400 to 3100 mm (Marengo 1998), with the highest monthly rainfall occurring from February to April (as high as 350 mm), and the lowest from June to September (as low as 180 mm). Despite thes e monthly differences, there is no real dry season (unlike more southern regions of the Peruvian Amazon). Monthly rainfall differences are reflected in the Yavar-Mir a nd Yavar River water levels and discharge. Water levels are lowest during the months of less rainfall (June to September), when sand beaches appear along the riverbanks. The Yava ri-Mir is a relativel y narrow black-water river, and could appear very shal low during the least-rainy months. The Yavar region harbors remarkable pl ant diversity. Althou gh vegetation in the study site is still poorly know n, about 1,600 plant species were identified during a recent rapid biological invent ory in the Yavar basin. Estimated total plant diversity in the region is as high as 2,500 to 3,500 species (Pitman et al 2003). This high diversity has led the whole area to be considered as one of the centers of plan t diversity (CPD) in South America (Smithsonian Institute 2003). The three main geomorphic units in the study area are terraces, alluvial plains, a nd sedimentary surfaces (Figure 2-1). Main habitat types in the area are upland forests a nd flooded forests. Upland forests cover most of the area, and exist on terr aces and sedimentary surfaces. They are not uniform through the area, with changes in plant compositi on occurring because of soil heterogeneity, somewhat similar to the upland forest around Iquitos (Ruokolainen & Tuomisto 1998; Pitman et al. 2003). Flooded forests exist on the all uvial plains of the Yavar-Mir and Yavar rivers. Swamp forests (a type of flooded forest) are common along these rivers,

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11 covering 25-50% of the flood plains (Pitman et al 2003), and occur also on poorly drained upland soils. Animal diversity in the area is also high, especially for mammals, causing some to consider the Yavar valley as one of the mammalian diversity hots pots of Peru (Valqui 1999, 2001; Salovaara et al 2003). Although there is some hunti ng in the area, it is slight compared to other sites in the Peruvian Amazon (Bodmer & Puertas 1999; Bodmer et al 2003), and many wildlife species are still abund ant. Lowland tapirs and other ungulates, for instance, have healthy populations at the Yavar-Mir River (Salovaara et al 2003). Methods An intense search for natural licks was conducted in the Yavari-Miri River valley from January to March 2001. This search oc curred along 66 km of trails opened on both sides of the river. Trails we re cut using predetermined bear ings, based on characteristics of the terrain observed from a satellite im age. Areas around the trails were checked carefully, especially when nume rous tapir tracks were found, si nce they often indicate the proximity of natural licks. Once a natural lick was found, its geographical coordinates were taken with a global pos itioning system (GPS), and marked on a 1:100,000-scale map. This search yielded 21 licks, most of them found on the north side of the YavariMiri River. Another 3 licks were found in Ju ly during a parallel study at the Yavari-Miri River (Salovaara, in prep.), and were included in our study. All 24 licks were located on the map (Figure 2-1). We monitored 7 to 24 licks from February to early December 2001 (except August), using 3 met hods: camera trapping, direct observation, and examining tracks.

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12 Camera Trapping Automatic 35-mm cameras triggered by a passi ve infrared motion detector were set at selected licks. From March to July, thr ee Buckshot passive infrared system cameras (Buckshot35, Louisiana, USA) were used. From September to early December, two additional CamTrakker (CamTrak South, Inc, Georgia, USA) cameras were available, for a total of 5 cameras used in our study. Ca meras were located at the entrance trails and/or in front of the most-u sed sites of the licks, to incr ease the chance of every lick visitor to be detected and photographed. Lo cations of the cameras were changed on average of every 2 weeks to allow sampling of several licks. A total of 14 licks was surveyed with 5 cameras (Table 2-1). Direct Observation At 7 licks, observation platforms (and so metimes blinds) were built to allow observation without being seen by the animals. The area of platforms was 2.2 x 2.2 m, and they were built 3 to 7 meters above the mo st-used sites of the licks. Palm leaves were put around the platforms, to make them less visible. Those licks were monitored from February or March through early D ecember 2001 (except August). An additional lick was added for direct observations from September, but no platform was built there. Instead, observations were made from a hammock tied 10 m above the lick. With the latter, a total of 8 licks was sampled by direct observation. On average, 3 licks were observed per m onth (range, 1 to 7). Diurnal and nocturnal observations were made at the licks. Tota l hours of observation were 796, of which 544 (68.3%) were nocturnal and 252 (31.7%) were diurnal. Total average observation time per lick was 68 h at night (range, 12 to 144 h), and 31.5 h during the day (range, 7 to 69 h) (Table 2-1). Diurnal observations were made with binoculars. Nocturnal observations

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13 were made with an ITT night vision scope. In some cases, a video camera was used to record animals visiting the licks. For each indi vidual entering the lick, we hand-recorded species identity, time of arrival and depa rture, and activity during the visit. Examining Tracks On average, 8 licks (range 5 to 13) we re checked for tracks every month from January to November 2001, except in June (when only 1 lick was checked) and August (when I was absent from the study site) (Table 2-1). We used this method to determine the proportion of licks used every month by la rge terrestrial species. When the same lick was checked for tracks more than once in the same month, we only used data for the first day of checking. Species ident ity was established from the animals tracks. Only fresh tracks inside the licks were re corded at the time of checki ng. This method is not suitable for arboreal animals (birds and arboreal ma mmals), and smaller terrestrial mammals (such as pacas and agouties); they are likel y to be underrepresented, especially when other larger animals step on the same entrance paths. Data Analyses Lick visitors An inventory of lick visitors was obtained by combining data from the three detection methods (camera trapping, direct observation and tracks). Frequency of natural-lick use Data from camera traps, direct observations and tracks were analyzed separately to describe the use of natural licks by wildlife species. Camera traps Frequency of lick visitation, as shown by camera trapping, was estimated as the number of captures (photos ) per 100 trap-nights (trapping success). A

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14 trap-night is defined as e ach 24-hour period in which camer as were operational. Overall trapping success was compared among species for the whole study period. Direct observation Frequency of lick visitation for each species (as shown by direct observation) was estimated as the number of sightings per 100 h of observation (sighting rate). Overall sigh ting rates were compared among species for the whole study period. Comparisons were done separately for bird and mammal species. Among mammals, comparisons were done for diurnal an d nocturnal species se parately. Also, for species with more than 10 observations, comparisons of lick visitation rates among seasons were done. Although, as mentioned abov e, seasonality in th e study area is not strong (a true dry season does not occur), the di fferences in rainfall and river levels led us to define three seasons: hea vy rainy season (from February to May), low rainy season (from June to September), and moderate rai ny season (from October to December). Since the sampling effort was not exactly the sa me for each season (Table 2-2), for each analyzed species, the expected frequency of lick visits was estimated by multiplying the total number of visits by the proportions of sampling effort from each season (weightedcount). Tracks For species detected with this method, the monthly rate of track occurrences was estimated as the ratio betw een the number of licks with tracks present over the total number of lic ks checked every month. Within each data set (camera trapping a nd direct observation), comparisons of lick visitation rates among species and/or among seasons were done with chi-square goodness-of-fit tests. Fo r all comparisons, a p -value 0.05 was considered significant.

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15 When comparing only two categories (species), Yates correction for continuity was used (Zar 1974). Lick-visitation rate and species abundance To test the null hypothesis that wildlife sp ecies visit natural lic ks in proportion to their abundance in the area, we used published informati on on abundance and density of large mammals coming from a 1,827-km line transect censuses conducted in the YavariMiri region from 1992 to 1999 (Bodmer et al 2003, Salovaara et al 2003). Data are available for several primates, ungulates and la rge rodent species. A chi-square test of homogeneity of proportions was used to co mpare the total number of sightings of mammal species (using only direct observation da ta), relative to their density in the area. Expected values for the test were obtain ed by multiplying the number of counts per species by the proportion of their density in the area. Birds were not included in this section because density data for most bird sp ecies are not available, except for large game species (Begazo 1999). Results Lick Visitors At least 7 species of birds and 15 species of mammals (a total of 21 species) were detected at the licks by camera traps, dire ct observation and track s (Table 2-3). Birds found using the licks were medium to large species and included 1 species of rail, 1 species of curassow, 2 species of guans, 1 sp ecies of pigeon, and 2 species of parakeets. Among mammals, lick visitors included 2 speci es of large primates, 4 species of ungulates, 4 species of medium to large rodents, 2 species of cats (ja guar and ocelot), and members of at least 2 families of bats. The cameras also captured a tail of an unidentified mammal (possibly a bushdog), which was excluded from analyses.

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16 Frequency of Natural-Lick Use Camera traps Sampling effort with camera traps totale d 412 trap-nights. That trapping effort provided 87 photographs of animals at 14 natu ral licks from March to early December 2001. Photos recorded at least 17 species ente ring the licks (Table 2-3). Half of the photographs (43) were bats captured at 2 licks (Table 2-4). Bats were common visitors in most licks year-round (from direct observation) However, at the be ginning of the study we noticed that they excessively triggered the cameras, reducing the time cameras were operational (on a single night a complete roll of film could be spent in only couple of hours). Cameras were moved away from high ba t-traffic areas, and thus bats may be underrepresented in camera trapping for the rest of the year. Use of licks by bats is mentioned in general, in the discussion belo w, but they were excluded from statistical comparisons. Most bats at the licks were l eaf-nose bats (Family Phyllostomidae), and at least 23% of the bat pictures were of fruit bats (Subfamily Stenodermatidae). Other than bats, the remaining 44 photogra phs showed 14 species visiting the licks (Figure 2-2). The overall lickvisitation rate (detected by camera trapping) was not the same across species ( 2 = 23.7, df = 13, p< 0.05). These differences in lick visitation hold when comparing only among mammals ( 2 = 15.5, df = 8, p< 0.05), but do not hold when comparing only among birds ( 2 = 2.1, df = 4, p> 0.05). Excluding bats, lowland tapir ( Tapirus terrestris ) was the most frequent species captured by the camera traps (10 photos in 412 tr ap-nights). Exclusive of pictures of the same individual, at least 8 di fferent tapirs were photogra phed at the licks. Tapir photos come from 5 of the 14 licks sampled with camera traps, which are located in the middle and upper Yavari-Mirin valley (Figure 2-1). Peccaries ( Tayassu pecari and Pecari

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17 tajacu ), deer ( Mazama americana ), pacas ( Agouti paca ), and ocelots ( Leopardus pardalis ) were captured 4 times at the licks, and the remaining species were registered only 1-2 times with camera traps. Direct observation A total of 119 animals were detected at the 8 licks sampled from observation platforms. Fifteen of the 21 species found at licks were seen with this method (Table 23). Eighty-three animals were observed duri ng day hours, and 36 animals were seen at night (Table 2-5). Over all sighting rate was not equal across species ( 2 = 88.3, df = 14, p< 0.05). Differences among species hold when comparing sighting rates among bird species ( 2 = 42.4, df = 5, p< 0.05), and among mammal species ( 2 = 42.5, df = 8, p< 0.05), separately. Among birds, pigeons ( Columba subvinacea ), parakeets ( Pyrrhura picta and Pionopsitta barrabandi ), and blue-throated piping guans ( Pipile cumanensis ) were the most frequent species at the lic ks, with sighting rates of 9.5, 4.7 and 4.3 sights per 100 observation hours respectively (Figur e 2-3.). Among diurnal mammals, black spider monkeys ( Ateles paniscus ) were the most frequent visitors, with a sighting rate of 5.1 sightings/100 diurnal-observation hours. Ho wler monkeys and the two species of peccaries and agoutis were seen also, but w ith less frequency (Figure 2-4.). Nocturnal visitors to the licks were tapirs, pacas, red-brocket deer, and in one occasion a porcupine. Red-brocket deer have both diurnal and noctu rnal activity, but they were grouped within the nocturnal mammals because they were seen at the licks only at night. Overall, tapirs were the most frequent visitors to the licks across nocturnal species with a rate of 3.8 sighthings/100 nocturnal-obser vation hours (Figure 2-5).

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18 Examining tracks A total of 24 licks were checked for tr acks throughout the year. Tracks of lowland tapir ( Tapirus terrestris ), white-lipped peccary ( Tayassu pecari ), collared peccary ( Pecari tajacu ), and red-brocket deer ( Mazama americana ) were found at the licks almost all year-around (Figure 2-6). However, rates of track occurr ences were higher for lowland tapirs, except in January. Data from June, although it is displayed, is excluded from this pattern because only one lick wa s checked for tracks that month. Track data indicate that even though a ll ungulates use licks during the year, tapirs visit a higher number of licks as compared to the ot her 3 species detected with this method. Variation in Lick Use through the Year Variation in lick use across the 3 seasons was determined only for the three most frequently observed bird species (pigeons, parakeets and piping guans) and the two most frequent mammals (spider monkeys and lowland tapirs). Although number of observations seemed higher after June, that wa s the result of an increase in the sampling effort. As a consequence, no significant differences were found when comparing the number of sightings in proportion to the hour s of observation across seasons for any of the species tested (Table 2-6). Lick-Visitation Rates and Species Abundance Density estimations in the Yavari-Miri River valley were available for the following mammalian species (Bodmer et al 2003, Salovaara et al 2003): spider monkey ( Ateles paniscus ), red-hower monkey ( Alouatta seniculus ), lowland tapir ( Tapirus terrestris ), white-lipped peccary ( Tayassu pecari ), collared peccary ( Pecari tajacu ), red-brocket deer ( Mazama americana ), and black agouti ( Dasyprocta fuliginosa ). Comparisons among species indicate that th ese mammals did not visit the licks in

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19 proportion to their abun dances in the area ( 2 = 795.15, df = 6, p< 0.05). Three patterns emerged from this comparisons: (a) species with low density and high visitation rate, such as tapirs, spider monkeys and howler m onkeys (Figure 2-7); (b) species with higher densities and lower lick visitation rate, such as the 2 peccary species ; and (3) species with both low densities and low lick vi sitation rate, such as the re d-brocket deer and the black agouti (Figure 2-7). Discussion Lick Visitors Birds The Yavari-Miri region harbors a large diversity of birds (Lane et al. 2003). The 7 bird species found visiting licks in the Yavari Miri River valley belong to 2 families of large birds (Rallidae and Cracidae) and 2 medium size birds (Columbidae and Psittacidae). Among the large birds, the fam ily Cracidae was the most common at the licks. Three of the 4 species of Cracidae inhabiting the Yavari region ( Crax salvini Penelope jacquacu and Pipile cumanensis ) (Lane et al 2003; Begazo 1999) were seen at the licks, and represent 75% of the species of this family in the area. They are large birds (>1.5 Kg) that use primarily in terior forest habitats (Beg azo 1999). Among the mediumsize birds visiting the licks, the most common (in fact the most frequent bird at the licks) was the pigeon ( Columba subvinacea ), one of the 6 species of the family Columbidae (16%) reported for this area (Lane et al. 2003). The other 2 bird species visiting the licks were 2 species of parakeets ( Pyrrhura picta and Pionopsitta barrabandi ), which are medium to small parrots, and account for the 10% of the parrot spec ies reported in the Yavari region (20 species) (Lane et al 2003). Large parrots and macaws were not observed at the licks, although they are reporte d using licks in othe r locations in the Amazon. That is also the case fo r large parrots of the genus Amazona and at least 3

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20 species of macaws ( Ara severa, A. chloroptera and A. macao ), seen at a natural lick along the riverbank of Manu River (Gilardi et al 1999, Emmons & Stark 1979) and Madre de Dios River (personal observat ion) in southern Peruvian Amazon. Most of these species are present in the Yavari-Miri region (Lane et al 2003, personal obser vation), but they were not sighted in the licks studied. An explanation for thei r absence in those licks is that large parrots are more common in open areas such as river pathways (Begazo 1999) and above forest canopy (Gilardi & Munn 1998) while the licks st udied were all found more than 1 kilometer inside the forest. The high cliffs along riverbanks of several Amazonian rivers, such as the Manu or Madre de Dios River, are not seen to the same extent on the smaller Yavari-Miri River. In contrast, use of licks by the Cracidae (guans) seems less common in the riverbank licks, than in the interior licks studied. This is expected since those cracid species prefer interior forest (Begazo 1999). All bird species observed at the licks we re engaged in geophagy, but the reasons for this behavior are not well understood. The several hypotheses proposed to explain geophagy in birds have been ex amined for parrots (Gilardi et al 1999), with evidence in favor of the detoxification hypothesis, a nd secondary, the mineral supplementation hypothesis. No information is available for th e other bird species in regard to geophagy. However, all the species at the licks have in common that they are frugivore (parakeets) or frugivore/omnivore (Stotz et al 1996), and may use licks for similar reasons. Independent of the specific benefits for the species, licks seem important for at least a set of large and medium bi rd species in the Amazon. T hose species, especially the cracids, although less dive rse than other bird groups, consti tute a significant part of the

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21 standing biomass of bird communities in the Neotropics (Terborgh 1986), and are important seed dispersers (Levey 1994). Mammals The Yavari region is also home for a large diversity of mammals; probably the highest recorded in any Amaz on location, and possibly even the entire Neotropics (Valqui 2001, Bodmer et al 2003, Salovaara et al 2003). Among the mammals, the most common lick visitors were 2 species of primates, along with most ungulates and large rodents. A lthough 13 species of primates exist in the Yavari-Miri valley, most of them are medium to small size primates, and only 3 species are large primates: the red-howler monkey ( Alouatta seniculus ), black spider monkey ( Ateles paniscus ), and the wooly monkey Lagothrix lagothricha ). Except for the latter, the largest primates were the one s seen at the licks in th is study. Although wooly monkeys are mentioned in one study as lick user s (Bicca-Marquez & Ca legaro-Marquez 1994), and at the study area were seen close to the licks on many occasions, they never actually came down to eat soil, as observed for howler and spider monkeys. Smaller primates such tamarins have been also reported eati ng soil (Heymann & Hartmann 1991), but more from termite mounds than natural licks. Seve ral species of howler monkeys and spider monkeys also are reported regular ly visiting licks in other tr opical forest of Colombia (Izawa 1993), French Guiana (Julliot & Sa batier 1993) and Br azil (Bicca-Marquez & Calegaro-Marques 1994). Ateles paniscus is a frugivoros primate, while Aloutta seniculus is more folivore species, although it includes fr uits and other food items in its diet. In general, no single reason for geophagy in prim ate species has been found (Krishnamani & Mahaney 2000), or for these two genera of large Neotropical primates in particular

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22 (Isawa 1993, Souza et al 2002), but all hypotheses suggest nutritional or medicinal benefits. All ungulates living in the Ya vari-Miri valley were seen at the licks, except for the gray-brocket deer ( Mazama gouazoubira ). Local inhabitants, how ever, report that this species is also a lick visitor, but their lo wer abundance compared to the other ungulates may explain why they were not detected during the study period. D eer and tapirs are browser/frugivore (Bodmer 1989), collared pecc aries are frugivore/omnivore, and whitelipped peccary are omnivore. Among rodents, the 2 large terrestrial rodents (paca and agouti) and one arboreal species (porcupine) use licks. The terrestrial rodents (paca and agouti) are also frugivores, a nd the arboreal one (porcupine) is a herbivore/frugivore. For ungulates it is suggested that use of licks is related to their nutrition or heath. The nutritional benefit hypothesis is examined in Chapter 3 and 4 for lowland tapir. Use of licks by other South American ungulates also is reported in other locations. For example, the Chacoan peccary also regularly visits licks (Sowls 1997), although its diet differs somewhat from the Amazonian species (Taber 1993). Other mammalian lick visitors were bats, mainly fruit-eating bats. These species were very common all year-around at the licks Little is known about the use of natural licks by fruit bats. Some information is ava ilable on bat mineral nutrition, but mainly for the Old World bats (Nelson 2003). Potential nutr itional benefits could be expected for the fruit-bat species observed in this study, and de serves more attention in future research. The family Phyllostomidae is the most di verse and common in th e Neotropics, and a substantial number of species ar e fruit-eating bats. Their role in the tropical forest as seed disperser is well known (Fleming 1988).

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23 Other than primary consumers at the licks, carnivores such as jaguars ( Panthera onca ) and ocelots ( Leopardus pardalis ) were also detected visiting these sites. There is no record of any carnivore eating soil, and the purpose of their visits is probably related to their prey, rather than a dire ct use of the soils at the licks Jaguars eat a variety of prey, including peccaries, pacas, agouties, a nd deer among other animals (Emmons 1987; Sunquist & Sunquist 2002). Ocelots eat smaller prey, weighing less than a kilogram such as spiny rats ( Proechimys spp.). Also, although not prominent in their diet, ocelots may occasionally kill agouties, deer and peccarie s (Sunquist & Sunquist 2002). All these prey species are lick visitors which may offe r an opportunity for easy hunting to these predators. In summary, a relatively large group of mammalian species and large bird species are lick visitors. Most of them are frugivor e or frugivore/herbivore species, and may obtain different benefits from the licks. Indirect benefits for non-herbivorous species are proposed for carnivores, since they may reduce their cost of foraging, by visiting the licks where prey may be concentrated. As a consequence, the use of licks also represents a cost for their herbivore users, since the risk of predation is high inside the licks. All these factors reveal that licks are an important component of Amaz on forest for a relative large number of species, and across the food guilds. Frequency of Lick Use From all the three method used in this study, the consistent pattern regarding differences in licks visitation rate indicate that lowland ta pir and spider monkeys, among mammals, and pigeons, parakeets and guans, am ong birds, are the most frequent lick users. No seasonality was found in their use of licks. This result contrasts with more seasonality in lick use reported in other sites, such as eastern Brazilian Amazon (Ayres &

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24 Ayres 1979) and southern Peruvian Amazon (M ontenegro 1998). Those sites are clearly more seasonal in terms of rainfall where differences between dry and wet season are stronger. Compared to those other sites, the Yavari-Miri River valley showed lower visitation rates, at least for species with so me information. For example, at the Madre de Dios River in Southern Peruvian Amazon, wh ere seasonality is very strong, a very high visitation rate to the licks was recorded for lowland tapir during the dry season (Montenegro 1998), and red-brocket deer (Mon tenegro, unpublished data). In that study, almost 200 observations of lowland tapir were obtained in about 3 months, whereas in the Yavari-Miri valley, just over 20 direct observations were recorded during almost a year. Several factors may explain these differences. Besides the differences in seasonality, at the Madre de Dios River, the location of the study was at an ecotur ism site where tapirs were already habituated to human presence. At the Yavari-Miri Rive r, tapirs were in general more difficult to see, and the higher number of sightings occurred at those licks further inside the forest. Als o, although hunting it is slight compared to other locations in Peru, licks are one of the preferred sites to hung tapirs (Chapter 5). Tapirs in the YavariMiri valley seem to be more cautious when visiting licks, and may even return to their trail before entering a lick when an observe r is present. This behavior depends on the individual, and is probably influenced by the pr evious experience of tapirs at licks used by hunters. Despite these differences, the common pattern in licks observed at Yavari-Miri and Madre de Dios Rivers, is the relatively high number of lick users, with a higher visitation rate by the lowland tapir, over other species. Sp ider monkeys also used licks in Madre de Dios, but they seemed to prefer another lick, and since only one lick was regularly

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25 monitored in that site, comparisons with Ya vari-Miri are difficult. In summary, the most frequent lick visitors overall are the lowland tapirs, and th eir use of licks is constant through the year in th e Yavari-Miri region. Lick-Visitation Rate and Species Abundance Wildlife species in the Yavari-Miri region did not use licks in proportion to their abundance. Lowland tapirs had the lowest dens ity, and yet, were the most frequent lick visitors. Low density but high lick use wa s also observed by the spider monkeys and secondarily by howler monkeys. Interestingly, peccaries are very abundant in the area, especially white-lipped peccary, and even though peccaries use the licks, they do it with less frequency compared to tapirs. White-lippe d peccaries seem to perceive their habitat at a different scale than collared peccar ies (Fragoso 1998, 1999). Th ey might be using other licks, located farthe r away in the forest. Overall, natural lick visitors comprise a relatively large set of species. The most frequent visitors, both birds and mammals, ar e mainly large species that comprise a substantial part of the standing biomass in the Amazon forest. Many of them are frugivores or frugivore/herbivores that play an important ro le in the forest structure through seed dispersion. Although the benefits for the species may vary, licks are an important resource for a large number of speci es, and should be considered an indicator of habitat quality for those species, and a key element in western Amazonian forests Summary and Conclusions A relative large number of Amazonian animal s visit natural licks in the Yavari-Miri River valley, in the northern Peruvian Amazon. Most species were large birds and mammals. The most frequent species visiting th e licks was the lowland tapir. No strong seasonality in lick use was observed in the study area, as seems to occur in other tropical

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26 forest. Species did not visit licks in propor tion to their abundance in the area. Lowland tapirs have low density compared to the othe r ungulates in the Yava ri-Miri River valley, and yet, they were the most fre quent visitor of natural licks. Table 2-1. Sampling effort used in three det ection methods to determine the frequency of natural-lick use by wildlife in the Ya vari-Miri River Vall ey, during year 2001. Direct observation2 Month Camera trapping1 Diurnal Nocturnal Examining Tracks3 January --------5.0 February ---2.038.0 7.0 March 29.08.061.0 7.0 April 1.05.50.0 6.0 May 7.05.073.0 11.0 June 9.012.524.0 1.0 July 21.036.560.0 9.0 September 108.064.084.0 6.0 October 141.049.072.0 10.0 November 98.062.0120.0 13.0 December 2.07.512.0 --Total 412.0252.0544.0 24.04 1 Number of trap-nights (number of 24-hour periods when cameras were operational). 2 Number of hours spent at observation platforms. 3 Number of licks checked for tracks. 4 Cumulative number of licks checked at the end of the study period. Table 2-2. Sampling effort used in direct observation per season. h = cumulative hours of observation. Direct observation Season Day (h) Night (h) Heavy rainy (Feb-May) 21 172 Low rainy (Jun-Sep) 113 168 Moderate rainy (Oct-Dec) 118 204 Total 252544

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27 Table 2-3. Species detected at natural lick s by camera trapping, direct observations and tracks in the Yavari-Miri Ri ver valley, Peruvian Amazon. Species English name Local name Camera traps Direct observation Tracks BIRDS GRUIFORMES Family Rallidae Aramides cajanea Grey-necked wood-rail X CRACIFORMES Family Cracidae Crax salvini Salvin's curassow Paujil X X Penelope jacquacu Spix's guan Pucacunga X X Pipile cumanensis Blue-throated pipingguan Pava negra X X COLUMBIFORMES Family Columbidae Columba subvinacea Ruddy pigeon Paloma X X PSITTACIFORMES Family Psittacidae Pyrrhura picta Painted parakeet Lorito X Pionopsitta barrabandi Orange-cheeked parrot Lorito X MAMMALS CHIROPTERA Subfamoly. Stenodermatidae Fruit-bats Mashu X Other Phyllostomidae Bats Mashu X X PRIMATES Family Cebidae Alouatta seniculus Red howler monkey Coto X Ateles paniscus Black spider monkey Maquisapa X CARNIVORA Family Canidae Speothos venaticus* Bushdog X Family Felidae Leopardus pardalis Ocelot Tigrillo X Panthera onca Jaguar Otorongo X PERISSODACTYLA Tapirus terrestris Lowland tapir Sachavaca X X X ARTIODACTYLA Family Tayassuidae Tayassu pecari White-lipped peccary Huangana X X X Pecari tajacu Collared peccary Sajino X X X Family Cervidae Mazama Americana Red-broket deer Venado rojo X X

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28 Table 2-3 (continued) Species English name Local name Camera traps Direct observation Tracks RODENTIA Family Erethizontidae Coendou prehensilis Porcupine Erizo X Family Agoutidae Agouti paca Paca Majs X X X Family Dasyproctidae Dasyprocta fuliginosa Black agouti Auje X X Family Echimidae Proechimys sp. Spiny rat Sachacuy X Probable. Table 2-4. Number of monthly photo-capture s at 14 licks form March to December 2001, in the Yavari-Miri Rive r Valley, Peruvian Amazon Season Species Heavy rainy Low rainy Moderate rainy Total Mar Apr May Jun Jul Sep Oct Nov Dec BIRDS Aramides cajanea 1 1 2 Crax salvini 1 1 Penelope jacquacu 1 1 2 Pipile cumanensis 2 1 3 Columba subvinacea 4 4 MAMMAL S Subfamiliy Stenodermatidae 7 10 17 Other Phyllostomidae 16 9 1 26 Leopardus pardalis 3 1 4 Panthera onca 1 1 Tapirus terrestris 1 1 4 3 1 10 Tayassu pecari 4 4 Pecari tajacu 1 1 2 Mazama Americana 2 2 4 Agouti paca 4 4 Dasyprocta fuliginosa 1 1 Proechimys sp. 1 1 Number animal photos 24 0 0 0 1 30 14 17 0 86 Trapping effort (# trap-nights) 29 1 7 9 21 108 141 94 2 412

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29 Table 2-5. Frequency of birds and mammals observed at eight natural licks from February to early December (excl uding August), 2001 in the Yavari-Mirin River Valley, Peruvian Amazon. Time of observation/Species FebMarAprMayJun Jul SepOct Nov DecTotals Day Birds Crax salvini 1.0 1.0 Penelope jacquacu 1.0 2.0 2 5.0 Pipile cumanensis (1-5) 1.0 1.0 4.0 2.0 4 12.0 Columba subvinacea 2.0 5.0 5.0 8.0 4 24.0 Pyrrhura picta* (>50) 1.0 5.0 3.0 2 11.0 Pionopsitta barrabandi* (>20) 1.0 1.0 Mammals Alouatta seniculus (5) 1.0 1.0 3 5.0 Ateles paniscus (2-3) 1.00 1.0 1.0 5.0 5 13.0 Tayassu pecari (>50) 1.0 1.0 1.0 1.0 4.0 Pecari tajacu (2) 1.00 1.0 1.0 3.0 Dasyprocta fuliginosa 1 2.0 1.0 4.0 Diurnal sightings/month 3.0 2.0 0.0 1.0 5.0 9.0 21.022.0 20 0.0 83.0 Day hours/month 2.0 8.0 5.5 5.0 13.0 36.5 64.0 49.0 62 7.5 252.0 Sighting rate (Sights/day hours) 1.5 0.2 0.0 0.2 0.4 0.250.330.45 0.32 0.0 0.33 Nigth Mammals Tapirus terrestris 1.0 2.0 3.0 2.0 4.0 4.0 5 21.0 Mazama Americana 2.0 1.0 1.0 1.0 1 6.0 Agouti paca 1.0 3.0 2.0 1.0 1.0 8.0 Coendou prehensilis 1.0 1.0 Sightings per month 2.0 6.0 0 5.0 3.0 3.0 6.0 5.0 6 0.0 36.0 Day hours/month 38.0 61.0 0 73.0 24.0 60.0 84.072.0 120 12.0 544.0 Sighting rate (sights/night Hours) 0.050.1 0 0.07 0.1 0.050.070.07 0.05 0.0 0.07 Total sightings 119.0 Total observation hours 796.0 Overall sighting rate (total sights/total Hours) 0.15 Sightings of groups, not individua ls (group size in parenthesis).

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30 Table 2-6. Chi-square values for testing th e null hypothesis that number of sightings is the same in the three seasons. Species 2 df p -value Birds Columba subvinacea 2.194 2 >0.05 Pyrrhura picta 1.152 2 >0.05 Pipile cumanensis 0.053 2 >0.05 Mammals Ateles paniscus 5.037 2 >0.05 Lowland tapir 3.131 2 >0.05 Figure 2-1. Location of 24 natural licks found in the Yavari-Miri RiverValley, northeastern Peru.

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31 00.511.522.53Crax salvini Aramides cajanea Penelope jacquacu Pipile cumanensis Columba cayannensis Proechimys sp. Dasyprocta Panthera onca Pecari tajacu Leopardus pardalis Agouti paca Mazama americana Tayassu pecari Tapirus terrestris Photo-captures/100 trap-nights Figure 2-2. Photo-captures pe r 100 trap-night per species at 14 licks from March to December 2001 in the Yavari-Mirin River Valley, Peruvian Amazon (excludes bats). 0246810Crax salvini Pionops itta barr abandi Penelope jacquacu Pyrrhura picta Pipile cumanensis Columba subvinacea Sighting rate (Sights/100 diurnal-observation hours) Figure 2-3. Total sighting rate of bird species at 8 licks surveyed from February to early December 2001 in the Yavari-Miri River Valley, Peru. Birds Mammals

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32 0123456 Pecari tajacu Tayassu pecari Dasyprocta fuliginosa Alouatta seniculus Ateles paniscus Sighting rate (Sights/100 diurnal-observation hours) Figure 2-4. Total sighting rate of diurnal mammal species at 8 licks surveyed from February to early December 2001 in the Yavari-Miri Valley, Peru. 012345 Coendou prehens ilis Mazama americana Agouti paca Tapirus terrestris Sighting rate (Sights/100 nocturnal-observation hours) Figure 2-5. Total sighting rate of nocturnal mammal species at 8 licks surveyed from February to early December 2001 in the Yavari-Miri Valley, Peru.

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33 0 0.2 0.4 0.6 0.8 1 JanFebMarAprMayJunJulSepOctNovRate of track occurrences (Licks with tracks/licks checked) Tapirus terrestris Tayassu pecari Pecari tajacu Mazama americana Figure 2-6. Ratio of track occurrences for tapir ( Tapirus terrestris ), white-lipped peccary ( Tayassu pecari ), collared peccary ( Pecari tajacu ), and red-brocket deer ( Mazama americana ) from January to November of 2001 in the Yavari-Miri Valley, Peruvian Amazon. 0 2 4 6 8 10 12 14 16A louat t a s e niculus Ateles p ani s cus Tapirus terrestr i s T ayassu p ecar i Pecari tajacu Mazam a am er icana Das y pr o cta f uli ginosaDensity (Ind./km2)0 0.01 0.02 0.03 0.04 0.05 0.06Lick visitation rat e (Sights/hour) Density Sighting rate Figure 2-7. Density of selected mammals in the Yavari-Miri Rive r valley and their overall lick-visitation rate during year 2001.

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34 CHAPTER 3 NATURAL LICK SOILS AS SOURCE OF MINERALS FOR WILDLIFE IN THE YAVARI-MIRI REGION Introduction Soils indirectly influence nutrition of herbivores thr ough the amount and quality of plant biomass they produce. However, since many animals purposely consume or lick soil materials (a behavior known a geophagy), a mo re direct effect of ingested soils is also considered (McDowell 2003). Many w ildlife species engage in geophagy, and diverse studies link this behavior to th eir mineral nutrition (Hebert & Cowan 1971; Weeks & Kirkpatrick 1976; Robbins 1983; Stark 1986; Jones & Hanson 1985; Klein & Thing 1989; Moe 1992; Kennedy et al .1995; Tracy & McNaugthon 1995; Holdo et al. 2002). Other researchers, however, associate soil ingestion with the potential benefits of clay in soils, such as buffering gastrointest inal fluids (Oates 19 78), avoiding diarrhea (Mahaney 1993; Mahaney et al 1996; Mahaney et al 1997), or providing protection against toxic plant seco ndary compounds (Gilardi et al 1999). The latter two benefits have been suggested due, in part, to a higher content of clay of some geophagical soils as compared to non-consumed soils. Geophagy is usually selective, occurring in specific locations commonly termed natural, mineral, salt or clay licks, de pending on the benefits attributed to soil consumption. Characterization of soils from natu ral licks is available for several sites of North America (Jones & Hanson 1985; Kennedy et al. 1995; Tracy & McNaughton 1995). In the tropics, chemical features of licks are ava ilable for Old World tropical

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35 savanna habitats (Weir 1972; Ruggiero & Fay 1994; Holdo et al 2002), and to a lesser extent, for tropical fo rest sites (Klaus et al .1998; Moe 1993). In the Amazonian Neotropics, natural licks have been characterized for a few sites, such as southern Peru (Emmons & Stark 1979; Gilardi et al 1999), a site in Brazil (Ayres & Ayres 1979) and southeastern Colombian Amazon (Narv aez & Olmos 1990; Lips & Duivenvoorden 1991). Results from the above studies vary, a nd comparisons are difficult because of differences in methods (including chemical determinations), number of natural licks sampled, presence/absence of control samples and their collection site with respect to licks, types of licks studied, geographical location, animal species using the licks, and general research questions, among others. Also, natural licks around the world have different origins and characteristics, and the be nefits to wildlife ar e obscured by regional differences in soil properties. For these reason s, it is necessary to consider not only the chemical composition of the licks, but their geoecological context in order to better interpret their role in th e ecology of their users. In tropical areas with high rainfall, some elements are easily leached and usually pose a challenge for the mineral nutrition of many wildlife speci es (Robbins 1983). One of the regions where such limitation exists is the Amazon basin, where precipitation is high, ranging 2000-3000 mm annually (Marengo 1998). Most of the Amazon forest is characterized as having very acid soils, low in available nutrients, and high in concentrations of toxic Al. In this type of environment, herbivore species may face mineral limitations if their only source of mine rals is the plant resources. If natural licks in the Amazon region provide some minerals of nutritional importance for herbivores,

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36 they might play an important role in animal nutritional ecology and population persistence. A region in the Amazon where natural licks occur and where many species persist in healthy populations is the Yavari-Miri River valley, in northeastern Peru (Salovaara et al 2003). A relatively high number of wildlife species use natural licks in the YavariMiri River valley (Chapter 2), including all resident ungulates (especially lowland tapirs), two species of monkeys, large rodents and large birds. It is unknown whether all these species are attracted to the licks for the same reasons. Ho wever, it is thought that for the herbivores in particular, lic ks might provide some elemen ts of nutritional importance. Also, it might be that those licks provide other, not necessarily exclusive, benefits to the animals, such as clay, as suggested for other Amazonian licks (Gilardi et al 1999). The purpose of this chapter is to describe the natural licks occurring in the middle Yavari-Miri River valley of the Peruvian Amazon in terms of their size and location along the river, and to evaluate them as a s ource of minerals and/ or clay for Amazonian herbivores. The hypotheses examined in this study were the following: Hypothesis 1 Soils at natural licks have higher mineral concentration (for one or more minerals) than non-lick soils. Hypothesis 2 .There is no difference in soil mi neral content between high water and low water seasons. Hypothesis 3. Lick soils have higher clay cont ent as compared to non-lick soils. It is predicted that if natural licks in th e Yavari-Miri River valley are a direct source of minerals, higher concentrations of one or mo re extractable elements will occur in lick soils as compared to non-lick soils. Also, if na tural licks are a reliable source of minerals through the year, it is predicted that their mineral concentrations (at least for some

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37 elements) do not substantially drop throughout th e year. Also, if animals are attracted to the licks for their clay content, it is predicted that higher pe rcentages of clay content will differentiate lick form non-lick soils. To te st these predictions comparisons of several physical and chemical characteristics of lic k and non-lick materials were conducted and analyzed within the regional geo-ecological context. Study Site The study was conducted along the Yavar-Mir River, a tributary of the Yavar River, in the Department of Loreto, in northeastern Peru. Fieldwork was conducted throughout the middle course of the Yava ri-Mir River, in the area between 4o30.23S, 72o26.69W and 4o24.77S, 72o09.76W. This area is located from San Cristobal Creek upstream to Maquisapay Creek (Figure 3-1). El evation in the area covered in this study varies from about 90 to 120 meters above s ee level. Mean annual temperature in the region is 26oC, with monthly mean maximum temperatures ranging from 28 to30oC, and monthly mean minimum from 17 to 20oC. Mean annual precipitation ranges from 2400 to 3100 mm (Marengo 1998), with the highest monthl y rainfall occurring from February to April (as high as 350 mm), and the lowest fr om June to September (as low as 180 mm). In spite of these monthly differences, there is no real dry season, as occurs in more southern regions of the Peruvian Amazon. Monthly rainfall differences are, however, reflected in the Yavar-Miri and Yavari river water levels and discha rge. The water levels are the highest during the months of heavy rainfall (February to April), and this period will be called here the high water season. The lowest water level of the Yavari-Miri River occurs during the months of less rainfall (June to September), when sand beaches appear along some riverbanks. The Yavari-Miri is a black water river relatively narrow, and

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38 could appear very shallow during the least rai ny months. This latter period will be called here the low water season. Geology of the Yavari-Miri valley is not known in detail, bu t research conducted around the Iquitos area (Rsnen et al 1998), and along the Amazon River (Hoorn 1993) provides useful regional information. The main geological formation in the area is the Pebas formation, a thick layer of sediments covering a large area of northern Peru, and equivalent to sediments of northwestern Br azil and southeastern Colombia (Hoorn 1993). The area is also associated with the Iquito s Arch, an uplifted geol ogical structure that separates the Amazon and Maraon Se dimentary basins (Hoorn 1993). The three main geomorphic units in the study area are terraces, alluvial plains and sedimentary surfaces (Figure 3-1). Main habi tat types in the area are upland forests and flooded forests. Upland forests cover most of the area, and exist on terraces and sedimentary surfaces. They are not uniform throughout the area, but change in plant composition because of soil heterogeneity, some what similar to the upland forest around Iquitos (Ruokolainen & Tuomisto 1998; Pitman et al 2003). Flooded forests exist on the alluvial plains of the Yavar-Miri and Yava ri rivers. Swamp forests, a type of flooded forest, are common along these rivers, coveri ng 25 to 50% of the flood plains (Pitman et al. 2003), and occur also on poor ly drained upland soils. Plant and animal diversity in the area is very high (Pitman et al 2003). The high mammalian species richness leads some to c onsider the Yavari valley as one of the mammalian diversity hotspots in Pe ru (Valqui 1999, 2001; Salovaara et al 2003). Although there is some hunting in the area, it is slight comp ared to other sites in the Peruvian Amazon (Bodmer & Puertas 2000; Bodmer et al 2003), and many wildlife

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39 species are still abundant. Lowl and tapirs and other ungulates, for instance, have healthy populations at the Yavari -Miri River (Salovaara et al 2003). Methods Lick Location and Description From January to March 2001, an intensive search for natural licks was conducted along 66 km in trails on both sides of the Yava ri-Miri River. Trails were cut across the 3 landscape units of the area (flood plains, terra ces and sedimentary su rfaces), and across an area of approximately 220 km2. This search yielded 21 natu ral licks. Three additional licks were found in July during a parallel re search project at the Yavari-Miri River (Salovaara, in prep.), for a total of 24 lic ks found from the San Cristobal Creek to Maquisapay Creek. Once a natural lick wa s found, its geographical coordinates were taken with a global positional system (GPS), and marked on a 1:100,000-scale map. Licks were measured (length and width) and described in terms of their form, number of geophagical sites (spots where an imals eat soil) and ge neral features of vegetation cover. Location of licks was displa yed on top of a satell ite image of the study area using the software ArcGIS to determ ine their distance to the river and the physiographic unit where they occurred. Physical and Chemical Charac terization of Lick Soils Soil sampling Soil samples from 7 licks were collected both during the high water season (March April), and the months of low rainfall or low water season (September-October). At each lick, 1 to 2 composite samples were collected from the sites where animals ate soil, plus a composite control sample from areas within 10 to 20 m outside of each lick. Each composite sample was made up from 3 to 4 sub-samples. Additionally 6 licks were

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40 sampled (lick and nearby non-lick soils) in September through November 2001, for a total of 13 natural licks sampled in those months. For the whole year, a total of 55 samples was collected (35 lick soil samples a nd 20 control samples, Table 3-1). Each sample (about 1 kg) was air dried and stored for further analysis. All natural licks sampled also were monitored for animal activity with one or several methods (Chapter 2). Laboratory analyses Samples were sent for analysis to the Terrapreta Soil Laboratory, a private laboratory in Colombia. Chemical characte rization of soils was conducted using the methods described by IGAC (1990) and included the following: soil texture, pH, organic C, available P, exchangeable Al, carbonates (CO3), cation exchange capacity (CEC), and extractable Ca2+, Mg2+, K+ and Na+. Samples collected during the high water season also were analyzed for concentration of B, Cu, Fe Mn, Zn and S. Percentages of sand, silt and clay in soil samples were determined by the Bouyoucos hydrometer method. Soil pH was measured with a potentiometer in a volumetri c 1:1 soil: water suspension. Organic carbon was determined by the Walckley-Black me thod, which uses chromic acid to measure oxidisable organic carbon in soil (Walkley & Black 1934; IGAC 1990). Available P was measured with the Bray II method, in whic h P is extracted using Bray II solution and measured colorimetricly, based on the r eaction with ammonium molybdate (Bray & Kurtz 1945; IGAC 1990). Exchangeable Al wa s determined by the Yuans method in KCl extractions (Yuan 1959; IGAC 1990). Carb onate concentration was qualitatively measured by reaction with 10% HCl. Cati on exchange capacity and exchangeable Ca2+, Mg2+, K+ and Na+ were extracted with 1N ammonium acetate at pH = 7. B, Cu, Fe, Mn, Zn and S were extracted with acid solutions of HCL and H2SO4. Concentrations of these elements in extracts were determined by atomic absorption spectrophotometry.

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41 Data analysis Since samples from each lick were matc hed with non-lick samples from nearby areas, differences in element concentrati ons between lick and non-lick samples were tested within seasons using paired t tests (Zar 1974). Likewise, differences in element concentrations between high wate r and low water seasons were te sted with paired t tests, using data from only those licks that were sa mpled in both seasons. For the latter tests, comparisons were made among licks and non-lick samples separately. Since the paired t test requires that differences among related sa mples have a normal distribution, a test for normality was conduced for each data set using the Kolmogorov-Smirnov test for normality. All tests for normality were non-significant, and no data transformations were needed to reach norma lity. For all tests, a p -value <0.05 was considered significant. All statistical analyses were pe rformed with the software SPSS version 11.5 for Windows. Results Lick Location and Description Most natural licks found at the Yavari-Mir i River, between San Cristobal Creek to Maquisapy Creek, where located in the area on th e northwest side of the river. Only 1 natural lick (lick number 14) was located on the right side of the Yavari-Miri River, on its flood plain. Distance to the licks from the river varied from 0 m (at the river bank) to 5,400 m in the upland forest (Table 3-2). Licks were located at elev ations varying from 92 116 m. The majority of licks (18 or 75%) were located on the sedimentary plain, and the remaining 6 (25%) were located on th e Yavari-Miri River flood plain (Table 3-2, Figure 3-1). No lick was found on terraces. Natural licks were classified according to their location as the following 4 types: (1) upland licks, (2) low bajial licks, (3) high bajial licks, and (4) river bank licks.

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42 Upland licks (n = 18) were located on th e sedimentary plain, in an upland forest environment that does not flood at any time of the year. These licks occur in forest openings, usually in depressions 3 10 m dee p, often with large stones, and caves made by constant mining of the anim als. Numerous animal teeth marks on the carved holes are present, and are accessed by clear animal path s. Most of these licks are close to small creek headwaters. Vegetation cover inside thes e licks is scarce, represented by some palm trees, shrubs and some ferns scattered on muddy surfaces. Low bajial licks (n = 2) were located on low flooded plains th at are inundated for several months during the high water season. They were located in low areas with poor drainage, from a few up to 400 meters away from the riverbank. This type of lick is functional only during the drier months of the year (June to September), and even in those months, may become flooded for several days after a heavy rain. Vegeta tion inside those licks is mainly herbaceous with scattered bushes on a muddy, soft surface. High bajial licks (n = 3) were also located on the flooded plain of the Yavari-Miri River, but unlike low bajial ones, they are flooded for shorter periods of time (approximately 30-40 days a year). They were located from 161 to 436 m from the riverbank (Table 3-2). Finall y, 1 riverbank lick was found on the YavariMiri River. Although a few more licks of this type exist along th e Yavari-Miri River, they were difficult to identify because they are underwater for several months of the year, and animal paths usually disappear with the flooding. Lick size varied from 10 m2 to 1,196 m2. Total area of licks added up to 7,282 m2. Total area of these licks re presents 0.0033% of the 220 km2 crossed by the trails. Although it is possible that some licks were mi ssed in the search, their proportional area is very small. Number of geophagical sites in side the licks varied from 1 to 3 depending

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43 on the size and form of the lick, with the la rgest licks having more than one geophagical site. Physical and Chemical Charac terization of Lick-Soils Particle size In lick soils, mean percentages of sand, silt and clay were 39.5 8.5 %, 41.5 6.9%, and 18.9 11.18%, respectively. In non-li cks soils, proportion of sand, silt and clay were 35 6.6%, 37.7 7.3 % and 27.22 7.6, respectively (Figure 3-2). Differences between lick and non-lick soils regarding pa rticle size proportions were not significant ( p >0.05). Texture of individual samples varied from loam to sandy loam, silt loam and clay loam. All textures were found in both li ck and non-lick soils. However, loam soils were the most frequent across all samples. Chemical properties of lick and nonlick soils Soil pH was higher in lick samples as compared to non-lick samples (Table 3-3), both in the high water season (t = 11.84, df = 6, p< 0.001), and the low water season (t = 7.74, df = 12, p < 0.001). In general, licks soils were e ither neutral or alkaline with a pH of 7 to 8, whereas non-lick soils were always acid, with pH of 3.5 to 5. Mean percentage of organic carbon vari ed from 0.6 0.27 % in non-lick soils to 1.26 1.03 % in lick samples (Table 3-3). Although organic carbon seems to be higher in lick soils, there was a large variation with in samples (range 0.3% to 3.7%), and differences were not significant in ei ther the high water (t = 1.18, df = 6, p = 0.28) or the low water season (t = 1.82, df = 9, p = 0.10). However, most samples, from both lick and non-lick soils had relatively low or ganic carbon, usually less than 1%. Exchangeable Al was very low in lick samples compared to non-lick samples in both seasons. In fact, only in th e low water season, some free Al+3 was found in lick soils,

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44 but in a much lower concentration th an in non-lick soils (t = 4.16, df = 6, p = 0.009), and none was found in the high water season (Table 3-3). In contrast, in non-licks soils, exchangeable Al varied from 11.65 to 12.88 meq/100 kg of soil. Cation exchange capacity varied on average from 21.88 4.32 to 25.22 5.76 meq/100 g of soil (Table 3-3), with no signi ficant difference betwee n lick and non-lick soils either in the high wa ter season (t = 0.78, df = 6, p = 0.46) or the low water season (t = 1.59, df = 12, p = 0.13). Lick soils had higher ba se saturation (many times over saturation) than non-lick soils (Table 3-3). Lick soils had higher content of P, Ca, Mg, and Na than non-lick soils, and those differences were consistent in both seasons (Table 3-3). Likewise, B, Cu, and S were present in higher concentrations in lick samples as compared to non-lick samples (Table 3-4). No significant differences between lick and non-lick soils were found for K, Fe, Mn and Zn concentrations ( p >0.05, Tables 3-3 and 3-4). Comp aring lick and non-lick soils between seasons, concentration of Ca in lick soils increased during the low water season (t = 6.4, df = 6, p = 0.001). Na concentration increased also during the low water season in lick soils (t = 2.49, df = 6, p = 0.047), and marginally in non-lick soils (t = 2.40, df = 7, p = 0.053), being always much hi gher in lick than non-lick samples (Table 3-3). No seasonal differences were found for P, Mg and K concentrations ( p >0.05) within each soil type. No seasonal comparisons were done for concentration of microminerals (B, Cu, Fe, Mn, Zn and S) because they were analyzed only in samples from the high water season.

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45 Discussion Lick Location and Description Location and other features of the natural licks at the Yavari-Miri River are related to the geological formations, landforms, and past and present tecton ic processes in the area. Researchers often associat e natural licks in this part of the Amazon with the Pebas formation (Lips & Duivenvoorden 1991; H oorn 1993). This formation is made of sediments deposited during the Middle Miocen e (11 to17 million years) in a long lasting, large shallow lake system with fluvial infl uence from the Andes, and occasional marine incursions from the Caribbean (Hoorn 1993; Rsnen et al. 1998). The Pebas formation is characterized by blue clay alternating with sand and lign ite layers with an abundant presence of fossil mollusks (Hoorn 1993). From a satellite image of the area, it is noted that main rivers in this part of the Amazon basin are controlled by a general lin ear pattern with a SW-NE orientation, dissected by smaller rivers running in a NW-SE lin ear pattern. These alignments form a tectonic micro-block pattern th at indicates neotectonic activit y. A similar pattern exists in the southern Colombian Amazon (IGAC 1999). B ecause of this neotectonic activity, the Yavari-Miri and Yavari Rive rs are being pushed up in a NW direction. As a consequence, terraces are formed to the SE of rivers, whereas on the NW side, the action is mainly erosive. This dynamic could be rela ted to fact that most licks were found on the NW side of the Yavari-Miri River, where eros ive activity is stronger. This fluvial erosion is probably associated with some of the rive rbank licks of the Yava ri-Miri River valley because it sporadically exposes the Pebas formation sediments. Riverbank licks, as named in this study, coincide with the barranco (cliff) licks described in the middle Caqueta region of s outhern Colombia, about 400 km north of the

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46 Yavari-Miri River (Lip s & Duivevoorden 1991). Also, some of the licks termed in this study as upland licks could coincide with the abandoned meanders (Lips & Duivenvoorden 1991), which are formed when old streams dissecti ng the sedimentary plain become dry during low water season. This latter type of lick is probably formed by a subterraneous flux of water enriched with elements leached form either sediments of the Pebas formation or sediments of differe nt origin. In fact, although most of the sedimentary plain is characterized by low mi neral content, superfic ial sediments can be very variable, with some having higher nutrient contents, depending on many factors (Linna 1993). Therefore, some licks may not be directly related to the Pebas formation, but could be associated with the flux of en riched water leaching superficial sediments. The names given to licks in this study (upland, high bajial low bajial and riverbank licks) reflect their location on the main landforms in the area, rather than their origin. This classification is arbitrary, with the intention to reflect their functionality through the year. Riverbank lic ks (especially if their lo cation is within maximumminimum water level), as well as low bajial licks are functional only when they are exposed, during low water season (from June to September-early October). Upland licks are more permanently functi onal since they do not become flooded at any time of the year. However, those licks ar e not static, but may occasionally lose their function, when new sediments cover the exposed materials that attract the animals. This dynamic, however, occurs on a larger time scal e, and thus is difficult to monitor in the short term. In the study area some old licks were found where the caves carved by the animals are still evident, but w ith no sign of recent use, and even with growth of pioneer

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47 plants. These considerations indi cate that contrary to what it may seem, natural licks are a dynamic resource. Licks in the study area were relatively small, compared to licks in other sites of the world, such those used by large mammals in Africa (Klaus et al. 1998) and Asia (Moe 1992). Licks in those parts of the world may act ually be very large, which is associated with the size and density of their users. The users of African licks, for example, are elephants and large ungulate s, some of which occur in high densities (Klaus et al 1998). The Amazonian licks are not as impressive in size, because their users are not as large as the African ones. However, in all these regi ons (Africa, Asian and the Amazon) the licks occupy a small proportion of the habitat, but ye t, are frequently used by many species. In this study, all ungulates, and several species of large rodents, large primates and large birds frequently use licks (Chapter 2), and even if they represent a small proportion of their habitat, they appear to be a very important resource fo r these species in the YavariMiri River valley. In other words, natural li cks in the study site may play an important role in the ecology of their users, di sproportionately to the area they occupy. Physical and Chemical Ch aracterization of Licks Particle size Natural licks did not show significantly high er mean clay content as compared to non-licks samples. This contrasts with findings in other licks of southern Amazonia in which clay content was 50% vs 35% in non-lick samples (Galetti et al 1999). In the licks in the Yavari-Miri region, mean clay content was about 19% vs 27% in non-lick samples, and the difference was not significant due to variation in both sets of samples. This percentage of clay content is considered medium according to the scale (15 to 40%) used by Kauffman et al (1998) for the upland soils around Iqu itos. Only 2 lick samples (out of

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48 32) were classified as clay (about 40% of clay ), and 5 were classified as clay loam (>28% of clay). The same textures were present in non-lick samples. Also, in the licks studied in the Colombian Amazon, 2 licks of the type called abandoned meander had high sand content (68-86% respectively) (Lips & Duiv envoorden 1991). In addition, 2 of the 3 soil samples consumed by mustached tamarins ( Saguinus mystax ) at the Rio Blanco, in northeastern Peruvian Amazon, were sandy a nd only 1 was fine-grained (Heymann & Hartmann 1991). Results of our study do not su pport the hypothesis th at it is the clay content that attracts animals to the licks, as may be the case for large parrots and macaws at licks in southern Peru (Gilardi et al 1999). These results agree w ith the view that there is not a single reason for geophagy across specie s. Most licks studied in the Yavari-Miri River valley were located inside the fore st, and large parrots or macaws were never observed in those licks, although they were observed flying above the tree canopy and along the Yavari-Miri River. Chemical properties of lick and nonlick soils Lick samples had the following differen ces with non-lick sa mples: higher pH, minimum free aluminum, and higher content of P, Ca, Mg, Na, B, Cu and S. These results coincide with other lick characteri zations in the Amazon region, in which more than one element is in a higher amount at the licks. For example, Ca, Mg, Na and sometimes K have been frequently more abunda nt in natural licks of Manu, in southern Peru (Emmons & Stark 1979; Montenegro 1998), middle Caqueta re gion of Colombia (Lips & Duivenvoorden 1991), and Amacayacu, in southern Colombia (Narvaez & Olmos 1990). In other tropical ar eas, like Africa, licks also show a high content of Na (Weir 1972; Abrahams 1999; Holdo et al 2002) and other elements, including Ca, Mg, P, and some times K (Klaus et al 1998; Ruggiero & Fay 1994; Hensahaw & Ayeni 1971;

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49 Tracy & McNaugthon 1995). In a few cases, howe ver, researchers have found it difficult to determine differences between lick and nonlick soils because of the large variation among samples (Seidensticker & McNeely 1975). An important factor in some studies has been the nature and origin of control samples, which may obscure actual differences of lick vs non-lick materials. Some times samples used as controls come from very distant sites from the licks a nd the regional variation of so il properties is seldom taken into account when doing comparisons. In temperate areas, licks used by large ungul ates are often rich in Na (Hebert & Cowan 1971; Fraser & Hristienko 1981; Klein & Thing 1989, Tankersley & Gasaway 1983; Miller & Livitaitis 1992). However, at a large scale some differences occur across the whole region. For example, in eastern Nort h America the main elements in licks are Na and Mg, whereas in western North Amer ica they are Ca and Mg (Jones & Hanson 1985). Since often more than one element is in higher concentrations at the licks, researchers find it difficult to attribute the use of licks to one single element as the one sought by the animals. However, it is important to consider that availability of one element in the soil is not independent to the other elements, as well as other properties of the soil. For this reason, in or der to better interpret the di fferences between lick and nonlick samples found in this study, it would be useful to consider not only the high concentration of some elements, but also other soil properties. Differences among lick and non-lick soils in this study fit in several aspects the characterization of 1 of 5 group soils described by Kauffman et al (1998) for the upland areas ( terra firme ) around Iquitos, 170 km west of the study site on the Yavari-Miri

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50 River. This group of soils (group I in Kauffaman et al. 1998) are young soils, not or slightly lixiviated, occurri ng on sites where erosion had exposed parental materials unaltered with meteorizable minerals such those of the Pebas formation or the named Buena Union unit (a unit described by the Amazo n River, close to the Iquitos area). Such soils are located in low areas (less than 200 m) or in transitional zones between upland forest and alluvial plain of the Amazon River or its tributaries. Th is group of soils has contrasting characteristics, w ith the upper part being very ac id, with low base saturation and high exchangeable aluminum. The same soil, at a depth between 2 to 3 m has a very high base saturation, no exchang eable aluminum, and neutral or slightly alkaline pH. The upper layer of these soils and the immediat e subsoil are porous and water permeable, whereas the deeper layer is water saturate d due to a low permeability. Clay and other textures are found in those soils. The above description coincides in many as pects with the features of the lick and their associated non-lick samples described in th is study. It is possible, then, that the licks in the Yavari-Miri valley ar e associated to a similar t ype of soils under comparable erosion processes. In the topsoil, when leaching removes Ca and other bases, pH reduces in approximately the same proportion (Brady 1974). At lower pH, more Al is free in the soil, reducing availability of other cations. So il materials less expos ed to leaching have higher pH, and consequently le ss free aluminum. Kauffman et al (1998) found that critical pH after which there is no interchange able Al in the soils of upland forest around Iquitos is 5.5. This coincides with the absence of free Al in the lick samples, since all of

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51 them had pH >5.5. As seen here, when pH is high, as in the lick samples, not only 1 but several cations (such as Na+, Ca2+, Mg2+ and K+) become more available. The presence of carbonates in the licks al so indicates that le ss altered parent materials are the constituents of the licks of the middle course of the Yavari-Miri River. For these reasons more than one elemen t (bases) are available at the licks. In general, nutrient availability in soils has been studied mainly in relation to plant nutrition, but not in direct association with animal nutrition. However, consumption of mineral-rich soil has been interpreted as a st rategy to alleviate mineral deficiencies or imbalances in the diet of some animal s. Evidence supporting the hypothesis that soil intake may help in reducing mineral defici encies was summarized by Kreulen and Jager (1984) and includes: (1) the ability of grazi ng livestock to choose supplemented salts containing elements that are deficient in their diets, (2) in vivo and in vitro experiments showing increase of macro and micronutrient levels in digestive liquors by elements released from ingested soil, and (3) incr ease in absorption and retention of several minerals by adding soil or clay to th e diet of some domestic animals. In southern Amazon, however, Gilardi et al (1999) did not find significant difference in the release of Na in an in vitro experiment by adding soil to an acid environment, simulating the parrots gut conditio ns, and concluded that lick soils were not a significant source of Na for the parrots, a lthough Na content was higher in lick samples. These researchers did not provide, however, information on the mineral content of the parrots diet, making it difficult to see whether other minerals could be of importance for the birds. Instead, they found s upport for the detoxification hypot hesis, in part because of higher clay content in lick samples. In contrast the natural licks we studied in the Yavari-

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52 Miri River valley did not show consistent di fferences in clay content, but they did consistently show higher concentrations of several elements as compared to non-lick soils. It is possible that more than one type of lick exists in the Amazon, and that they have different origins, and prope rties. The role of natural licks may vary across species as suggested by other researchers in severa l parts of the world (Kreulen 1985; Diamond et al. 1999; Klaus & Schmid 1998; Krishnamani & Mahaney 2000). Since the licks studied in the Yava ri-Miri River valley showed a higher concentration of several elements, it is possi ble for animals to exploit them according to their needs. Elements sought by animals w ill depend on the properties of their food, and especially their elemental con centrations. In Chapter 4, elem ent concentration in the food of the lowland tapir, the most frequent lick user in the Yavari-Miri River, is examined. Summary and Conclusions The purpose of this chapter was to descri be the natural licks occurring along the middle course of the Yavari-Miri River, and to establish whether they were a source of mineral nutrients and/or clay for herbivores. Another objective was to examine whether licks maintain their mineral concentration through the year. Most licks were located on sedimentary plains, and most s eem to be related to the deposits of the Pebas formation. Mineral content of licks was higher than nonlick samples, and did not drop through the year. Some elements such as Na and Ca even increased in concentration during the drier months, probably because leaching is reduced during those months. Several elements were available and potenti ally used by the animals in the YavariMiri River valley. Among macr ominerals, Na, Ca, Mg and P had consistently higher concentrations in licks than nonlick samples. This is relate d to the low alteration of the

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53 sediments that form the licks. Also, among microminerals, Cu, S and B were more concentrated in the licks. Overall, our results indicate that natural licks represent a source of minerals for wildlife in the Yavari-Mir i River valley. Whether animals use licks for one or more minerals would depend on the mi neral concentration of their food and their potential needs for specific elements, which probably varies across species. Further research is needed in order to examine the mineral concentration foods eaten by lick users in the Amazon forest. A study in this dire ction was conducted for one of the most frequent lick visitors, the lowland tapir (Chapter 4). Table 3-1. Number of soil samples from lick and non-lick sites gathered in year 2001 in the Yavari-Miri River valle y in the Peruvian Amazon. High water season Low water season Lick number Lick soils1 Non-lick soils2 Lick soils1 Non-lick soils2 1 2 1 2 1 2 2 1 2 1 11 2 1 2 1 12 1 1 1 1 13 2 1 2 1 15 2 1 16 2 1 3 1 18 2 1 19 2 1 1 1 20 1 1 21 2 1 22 1 1 24 1 1 Total samples 13 7 22 13 1 Number of licking sites inside each lic k; a sample was taken from each site 2 Matched control samples taken within 10-20 m outside the licks All samples (lick and non-lick soils) were composed of 3-4 sub-samples

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54 Table 3-2. Descriptive features of 24 natura l licks in the upper Yavari-Miri River valley, Peruvian Amazon. Location Coordinates Lick Number Latitude Longitude Distance from river (m) Elevation (m) PhU1 Lick type2 Size (m2) GS3 1 -04o22.16 -72o11.57 1,300109SP Upland 1,196 2 2 -04o22.10 -72o10.28 1,350104SP Upland 201 2 3 -04o22.70 -72o11.91 564109SP Upland 25 1 4 -04o21.90 -72o12.47 1,326109SP Upland 80 1 5 -04o22.54 -72o11.91 533116SP Upland 30 1 6 -04o27.43 -72o19.50 73394SP Upland 25 1 7 -04o27.30 -72o19.62 1,05094SP Upland 30 1 8 -04o27.69 -72o19.21 10094FP Low bajial 400 1 9 -04o26.58 -72o19.54 1,68594SP Upland 15 1 10 -04o26.80 -72o20.95 3,50094SP Upland 35 1 11 -04o26.17 -72o18.60 77092SP Upland 928 2 12 -04o30.47 -72o25.26 625109SP Upland 81 1 13 -04o30.73 -72o25.26 310112FP High bajial 293 2 14 -04o20.08 -72o10.93 586110FP Low bajial 100 2 15 -04o23.70 -72o15.19 500103FP High bajial 436 2 16 -04o23.11 -72o15.24 1,500103SP Upland 1,010 3 17 -04o30.80 -72o25.74 0111FP Riverbank 25 1 18 -04o29.79 -72o25.72 1,800112SP Upland 180 2 19 -04o29.78 -72o25.78 2,000112SP Upland 527 2 20 -04o25.51 -72o18.39 88097SP Upland 357 2 21 -04o24.50 -72o19.01 3,03097SP Upland 323 2 22 -04o23.56 -72o19.52 5,40097SP Upland 814 1 23 -04o30.62 -72o25.23 590111SP Upland 10 1 24 -04o30.67 -72o25.25 380100FP High bajial 161 1 Mean natural-lick size (sq meters standard deviation) 300 351 Total area of natural licks (square meters) 7,282 Licks sampled for soil analyses 1 PhU = Physiographic Unit; SP = Sedi mentary Plain; FP = Flood Plain. 2 Lick type: Upland = licks appear as depres sions in upland forests, usually with large stones and caves or mined holes; Low Bajial = licks are on areas flooded for several months; High bajial = licks are on areas interm ittently flooded for days to several weeks; Riverbank = licks are on the cliffs of th e Yavari-Miri riverbank, and are under water several months a year. 3 GS = Number of geophagical spots (where animals actively consume soil) inside each natural lick

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55 Table 3-3. Chemical characteriza tion of soils from lick and non-li ck sites in two seasons of year 2001 in the Yavari-Miri River valley in the Peruvian Amazon. 1 The value refers to the percentage of samples that had positive reac tion to 10% HCl, indicating th e presence of carbonates in the sample. No test SD = Standard deviation High water season Low water season Feature Lick Soils (n = 13) Non-lick Soils (n = 7) Paired t-test p -value Lick Soils (n = 22) Non-lick Soils (n = 13) Paired t-test p -value Mean SD Mean SD Mean SD Mean SD pH (1:1 soil:water) 7.41 0.54 4.61 0.63 6.95 0.82 5.15 0.61 Organic Carbon (%) 1.26 1.03 0.84 0.26 1.22 0.88 0.60 0.27 Samples with CO3 (%)1 84.61 0 59.09 15.38 P available (ppm) 82.55 38.90 2.57 2.27 0.001 85.90 50.39 22.05 35.52 0.001 Al 3+ (meq/100 gr) 0.00 11.65 6.85 0.027 0.128 12.88 7.48 0.009 CEC (meq/100 gr) 21.88 4.32 23.32 5.87 22.46 4.33 25.22 5.76 Base Saturation (%) 97.6 to >100 57.9 13 79.3 to > 100 47.00 21.1 Extractable bases Ca2+ (ppm) 4114.00 941.00 1969 541.000.001 4385 1324 2031 1395 <0.001 Mg2+ (ppm) 720.00 326.00 375.00 202.000.001 764 355 338 168 <0.001 K+ (ppm) 75.49 32.57 65.91 29.47 0.520 99.88 30.80 86.92 31.53 0.333 Na+ (ppm) 67.82 44.90 6.87 4.39 0.014 102.74 57.92 17.79 9.94 <0.001

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56 Table 3-4. Microminerals in lick and non-lick soils during the high water season of 2001, in the Yavari-Miri River va lley in the Peruvian Amazon. Element Lick Soils (n = 13) Non-lick Soils (n = 7) Paired t-test p -value Mean SD Mean SD B (ppm) 0.32 0.20 0.13 0.04 0.006 Cu (ppm) 3.08 1.12 1.12 0.83 0.012 Fe (pmm) 95.51 69.73 55.81 29.06 0.156 Mn (ppm) 19.33 15.31 51.53 49.82 0.164 Zn (ppm) 2.17 0.99 1.39 .090 0.282 S (ppm) 141.74 153.93 6.79 3.91 0.020 Figure 3-1. Location of the study site in the Yavari-Miri River valley, in northern Peruvian Amazon.

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57 0 10 20 30 40 50 60 SandSiltClay Particle SizeContent in soil (%) Lick Non-Lick Figure 3-2. Mean content of sand, silt and cl ay in samples from lick and non-lick soils. Size of vertical lines indicat es 1 standard deviation.

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58 CHAPTER 4 BROWSE AND FRUIT AS A SOURCE OF MINERALS FOR LOWLAND TAPIR IN THE YAVARI-MIRI REGION Introduction Lowland tapir ( Tapirus terrestris ) is the largest wild terrestrial mammal of the South American tropics (Eisenberg 1989). Average adult weight varies from 150 to 300 kg, with females being slightly heavier th an males (Padilla & Dowler 1994, Emmons & Feer1997, Shoemaker et al 2004). Tapirs are odd-hoofed ungulates, and are related in their phylogeny to horses and rhinoceroses, sh aring with them several morphological and physiological characteristics. For example, like horses and rhinos, tapirs are nonruminants, and have a relatively simple stomach contrasting with a large cecum and a voluminous and enlarged sacculated colon (Stevens 1988), and have hindgut fermentation (Janis 1976). However, unlike hors es and some species of rhinos, tapirs are browsers/frugivores (Bodmer 1990), and live primarily in humid tropical forests. In several sites of the Amazon forest, es pecially in western Amazonia, lowland tapirs frequently visit natural licks (Pea et al 1996; Montenegro 1998), and may spend on average half an hour in geophagy (ingestion of soil materials) (Montenegro 1998). Lowland tapirs are the most frequent nocturnal species vi siting natural licks in the Yavari-Miri River region of the northern Peruvian Amazon (Chapter 2). This habit seems to be related to the tapirs nutritional ecology. Analysis of consumed soils in the YavariMiri region revealed a higher concentration of se veral elements (P, Ca, Mg, Na, B, Cu and S) as compared to control samp les outside the licks (Chapter 3).

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59 One common hypothesis is that animals e ngaging in geophagy are under some kind of stress, often of nutritiona l nature. Several studies have investigated the chemical characteristics of the eaten so ils to identify which elements are in higher concentration at licks, in order to explain geophagy in some species (Emmons & Stark 1979; Jones & Hanson 1985; Tracy & McNaughton 1995). However, often more than one element is in higher concentration in consumed soils, maki ng it difficult to associate soil consumption to a particular mineral nutrient. Often, low levels of dietary sodi um in tropical areas explain geophagy in both wild and domes tic animals such as elephants (Holdo et al 2002) and cattle (McDowell 2003). In addition, several st udies have found that in temperate areas many ungulates also obtain Ca or Mg from licks (Jones and Hanson 1985). Also, some trace minerals such as Se a nd Co could be obtained from ingested soils (Grace et al 1996; Underwood and Suttle 1999). The nutritional importance of soils as a di etary source of minerals depends on the amount of soil ingested, the ratio of mineral concentration in soil to that of consumed plants, and in the ability of the animal to ex tract and absorb elements directly from the soil (McDowell 2003). For many wildlife specie s, however, information on the mineral concentration of their foods is unknown, making it difficult to identify potential mineral deficiencies or unbalances that could be driving animals to consume soil. Although the lowland tapirs diet has been st udied in several tropi cal locations such as Peru (Bodmer 1990), Brazil (F ragoso 1997; Olmos 1997; Fragoso et al. 2000; Galetti et al. 2001), Venezuela (Salas and Fu ller 1996), French Guiana (Henry et al. 2000), and Colombia (Pea et al. 1996), very little is known about th e nutritional contents of foods eaten by tapirs in the wild, except for some reports of fat, carbohydrate and protein

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60 content of several Amazonian fruits (Lopes et al. 1980). Also, mineral requirements and status of tapirs in the wild are unknown, making it difficult to identify any deficiency or unbalance that may be driving th em to visit natural licks. In captivity, tapirs are usually fed foll owing guidelines for horses, due to their similarity in digestive system anatomy (Barongi 1992; Janssen et al. 1999; Shoemaker et al. 2004). Those diets comprise legume hay, herbivore pellets and commercial produce and/or harvested browse plants, and mine ral supplementation when needed (Shoemaker et al. 2004). In the wild, however lowland tapirs feed on a large amount of fruits, relatively high for a herbivore of that size (Bodmer 1990). They also consume leaves and fiber (other plant parts such as stem s, bark or wood) (Bodmer 1990; Henry et al. 2000). Although estimation of percentage s of each of these 3 items may vary according to food availably, studies in the Amazon and French Gu iana have shown that at least 30% of the lowland tapirs diet is comprised of fruit, and the remainder made up of varying amounts of leaves and fiber (Bodmer 1990; Henry et al. 2000). In French Guiana, lowland tapirs may consume up to 70% of fiber (Henry et al 2000). It is unknown, however, whether lowland ta pirs can obtain all their necessary nutrients exclusively from food. Since lowland tapirs frequently visit natural licks that are rich in several minerals in the Yavari-Miri River valley, lowland tapi r food in this area might be limited in some elements. Since no seasonality was found in lick use in the Yavari-Miri region (Chapter 1), any potential nutritional limita tion in tapir food related to lick use is expected to be present all year around. An indirect way to examine potential defi ciency of one or more minerals is by examining fecal excretion of such minerals. Fe cal mineral content has been used in other

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61 herbivores as a method to examine minera l status, particularly for sodium (Khalili et al. 1992; Studier et al 1994), or absorption, particul arly for calcium (Schryver et al 1983). In cases of depletion, fecal excretion of some minerals (i.e. sodium and phosphorus among others) reduces considerably, in some cases virtually to zero (i.e. phosphorus) (McDowell 2003). If tapir food is limited in one or more mi neral nutrients throughout the year, very little excretion of such minera ls (at least for sodium and pho sphorus) is expected in feces, unless such limitation is alleviated by other sources. If tapirs cons ume mineral rich soils, naturals licks, may represent a critical re source for lowland tapir nutrition, and overall, their persistence in western Amazonia. The purpose of this chapter is to evaluate lowland ta pirs food as a source of minerals in the Yavari-Miri River valley. Th e main hypotheses examined in this chapter are the following: Hypothesis 1 Lowland tapir food is limited in one or more mineral nutrients in the Yavari-Miri River valley, and such lim itation is constant through the year. Hypothesis 2. Excretion of limited minerals (at least for some minerals) is low in tapir feces. To test these hypotheses, the diet of lo wland tapir in the Yavari-Miri River was studied, and the mineral content of the most frequently eaten foods was analyzed. Also, analyses of minerals in lowland tapir f eces were conducted to examine fecal mineral excretion. If lowland tapirs eat mineral rich soils at natural licks because of a mineral nutritional deficiency or unbalance, it is expected that: (1) on e or more elements in tapir food are low in comparison to mineral requirem ents of lowland tapi rs, (2) no significant changes occur in the mineral content of tapir food thr ough the year, and (3) mineral

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62 concentration of one or more minerals in tapi r feces would be higher than expected if the animals are facing a deficiency of such minerals. Study Area This study was conducted in the middle cour se of the Yavari-Miri River, in the Peruvian Amazon, in the area between 4o30.23S, 72o26.69W and 4o24.77S, 72o09.76W. Weather in the area is characteri zed by a mean annual temperature of 26oC, with mean maximum temperatures ranging from 28-30oC, and mean minimum from 1720oC (Marengo 1984). Mean annual precipitatio n varies from 2400 to 3100 mm, with the highest monthly rainfall occurri ng from February to April, a nd the lowest from June to September. The water levels are the lowest during the months of less rainfall (June to September), and the highest during the mont hs of maximum precip itation (February to May). Plant diversity in the area is very high. Recent estimates indicate that number of plant species in the Yavari region may reach up to 3,500 species (Pitman et al. 2003). Habitat types in the area in clude upland and flooded forests. Upland forests are very diverse and vary greatly with soil char acteristics (Roukolainen & Tuomisto 1993). Flooded forests tend to be heterogeneous a nd continually changi ng due to the river fluctuations (Puhakka & Kalliola 1993). Among flooded forests, swamp forest, is common along these rivers, covering 2550% of the flood plains (Pitman et al. 2003). Methods Lowland Tapir Diet in the Yavari-Miri Region Diet of lowland tapir in the Yava ri-Miri region was studied through both examination of feeding signs and inspection of tapir feces. A sear ch for tapir feeding signs was conducted along 26 trails opened on bot h sides of the Yavar-Mir River, from

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63 January to December 2001. Trail length varied from 2 to 5 km, for a total of 65.8 km of trails. Once a feeding sign was found, browse clearly eaten by tapirs was collected. When feeding on leaves, tapirs usually pull down branches and stems, leaving teeth marks on the bark (Salas & Fuller 1996), and very ofte n may cut the stem at about 1 m from the ground (usually when it is up to 2 cm in diam eter), leaving a charac teristic feeding sign of a broken stem with its upper part hangi ng down. When feeding on lower vegetation, especially from plants growing in gaps, ta pirs eat leaves from young plants up to 1.5 m above ground (personal observation), and the feeding sign is unmist akable. In addition, since tapirs also feed on fru its (Bodmer 1990; Olmos 1997; Henry et al. 2000), several fruits were collected from tapir feeding sites. In all cases, tapir feeding was confirmed by the presence of tapir tracks at the feeding site, and only browse or fruits undoubtedly eaten by lowland tapirs were collected. Composite samples from every browsed plan t were collected with stainless steel scissors and rubber gloves, and placed in co tton bags. Samples were air-dried for several days and stored in dry plastic bags until they were analyzed for mineral content. Also, a part of the fresh sample was prepared as botanical vouchers for sp ecies identification. Voucher samples were sun dried for severa l days and stored. Fruit samples were preserved in 95% ethanol in ti ght plastic containe rs until they were dried for mineral analyses later. Fruit samples were dried in an oven at 60oC for 24 hours prior to mineral analysis. Botanical vouchers were identified at the Herb arium Amazonense (AMZ) in Iquitos, Per. Voucher specimens were de posited at the same herbarium. Plant identification follows nomencl ature from Gentry (1996).

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64 Also, lowland tapir feces were collected al ong trails, from streams, and to a lesser extent, from tapir latrines. Fecal samples were sun dried for several days and stored for further analyses. All samples were handled wi th rubber gloves and placed in individual clean plastic bags. About 50 % the feces samples was examined for proportion and frequency of occurrence of food types (fruits, leaves a nd fiber), following Bodmer (1990), with the difference that no stomach samples were used in this study. The remaining 50% of the samples, mainly the most fresh, were left for examination of mineral content. Determination of Minerals in Tapir Food and Fecal Samples Browse, fruit and fecal samples were analyzed for concentration of nitrogen and 11 minerals: 6 macrominerals (P, K, Ca, Mg, S and Na) and 5 trace minerals (Mn, Zn, Cu, Fe, and B). Laboratory analyses were conducte d in the laboratory of soils, water and plant tissues of the Institute for Agricultu re (CORPOICA) in Colombia. Samples were pretreated (or mineralized) w ith a wet oxidation-digestion pr ocedure to remove organic matter. Reagents for this procedure were Ni tric and Perchloric aci ds in proportion 3:2. Digestion was conducted by graduall y increase of temperature at 100oC intervals up to 300-330oC approximately, in a Tercat or digester. Part of the resulting aqueous solution was completed with water and concentration of Fe, Cu, Mn, and Zn was determined in an atomic absorption spectrophotometer Perkin Elmer 2380. For determination of K, Ca, Mg and Na, lanthanum was added to another part of the aqueous solution and their concentration was determined also by atom ic absorption spectrophotometry. Phosphorus concentration was determined by adding a colorimetric reagent of ammonium and potassium tartrate, sulf uric acid, ammonium molybdate, an d ascorbic acid to the aqueous solution containing the minerals, reading the absorbance of the solu tion in a Milton-Roy

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65 light spectrophotometer, and comparing with a calibration curve. Sulfur concentration was determined also by spectrophotometry, af ter adding a solution of nitric and acetic acids and a turbidimetric reagent of bactogel and barium chloride to the aqueous solution containing the minerals. To determine Boron and Nitrogen content, non-digested samples were used. For B, 1 g of plant tissue was mixed with 0.1 g of calcium oxide and dry ashed in a muffle furnace at 500oC. Ashes were mixed with sulfuric acid, filtered and mixed with Azometin H for color development, and concentration of B was determined by spectrophotometry. Nitrogen was determined with the Kjeldahl method (Ma & Zuazaga 1942). Data Analyses Assumptions of normal distribution and hom ogeneity of variances were tested for all variables with the Kolm ogorov-Smirnov test and Lavenes test respectively. When assumption of normality was not met, altern ative non-parametric tests were used. For testing differences between 2 groups, t-test s or the Wilcoxon test were used. When comparing more than 2 groups, a one-wa y Analysis of Variance (ANOVA) or alternatively the Kruskal-Wallis test we re used. If differences were found when comparing more than 2 groups, further multip le comparisons were done with the Tukey test to find which groups we re different. For all tests, a p <0.05 was considered significant. Mean concentration of each mine ral in leaves was compared between high water and low water seasons. Also, mineral content of leaves was compared among the most common plant families in tapirs diet Mean concentration of each mineral was compared between leaves and fruits. Finally, mean concentration of each mineral in feces was compared to mean concentrations in both leaves and fruits separately. All statistical analyses were performed with the so ftware SPSS version 11.5 for Windows.

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66 Results Lowland Tapir Diet at the Yavari-Miri Region A total of 134 browse samples was collect ed from the forest on both sides of the Yavari-Miri River. Samples represent 31 plant families, 63 genera and 89 species (Table 4-1). The most common lowland tapirs br owse was from the Melastomataceae (22%) and Rubiaceaae (17%) families (Figure 4-1). The next most common families in tapir browse were Areaceae (6%), Myristicaceae (5%), Fabaceae (4.47%), and Sapotaceae (3.73%). The remaining species represented from <1% to 2.2 % of tapirs browse (Figure 4-1). A total of 72 tapir fecal samples was collected from January to December 2001. 80% of those samples were found in shallow water, along banks of small streams, while only 20% were found on the ground, in tapir la trines. Tapir latrines were found only twice in this study. A total of 37 fecal sample s were sent to the laboratory for mineral analyses. The remaining 35 samples were exam ined for determination of the components of tapirs diet. Fruit parts, leaves, fibers (stems, wood, and other fibrous plant materials), and soil were found in tapir feces. Percentage of occurrence of thes e items in feces was 96.6% for fruit parts, 100% for leaves a nd fibrous materials, and 76.6% for soil. Proportions of these items on a dry matter ba sis were the following: fruit parts 8.89 9.33% (range 0 43.75%), leaves 75.42 16.91% (range 18.09 90.22%), fibers 12.54 13.27 % (range 2.17 68.09%) and soil 3.20 3.14% (range 0 8.42%). The proportion (on a dry weight basis) of fruit in tapir diet is underrepresented. A ll but one fecal sample analyzed for diet components had fruit remain s (exocarps and seeds), but their weight was comparatively low because the largest seed s are spit out and are not in the feces,

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67 although the pulp was consumed in large amount s. This was observed in other studies where stomach contents were analyzed (Bodmer 1990; Henry et al 2000). In consequence, real proportion of fruit in tapir diet in the Yavari-Miri River is higher than the average shown above. Tapirs ate at least 14 fruit species (Tab le 4-3). The most common fruits found in tapir feces and their percentages of occurrence were the following: Mauritia flexuosa (70%), Annona spp (40%) Spondias mombin (40%), Oenocarpus bataua (35%), Couma macrocarpa (25%), and Attalea sp. (15%) (Figure 4-2). Also from feeding signs along tapir trails, we found that frui ts of a species of Moraceae ( Ficus insipida ) are also part of the tapirs diet (Table 4-3). Minerals in Lowland Tapir Food Concentration of minerals in lowland tapirs browse was analyzed in 37 leaf samples, representing 32 species (Table 4-1). Analyzed samples included the most common species browsed by lowland tapirs. Me an concentrations of macrominerals (P, K, Na, Mg, S and Na) and trace elements (M n, Zn, Cu, Fe and B) in tapir browse are illustrated in Figures 4-3 and 4-4, respectiv ely. No seasonal differences were found in macromineral concentra tion in tapir browse ( p >0.05 in all tests), except for a barely significant difference in P during th e low water season (t =2.05, df=35, p =0.047) and a higher concentration of Mg during th e high water season (t = 2.2, df = 35, p = 0.034). Although K seems to be at higher concentrations in the low water season, there was large variation among samples, and the statistical test was not significant (Wilcoxons test z = 0.68, p = 0.50). Among trace elements, only Fe (t = 2.3, df = 35, p =0.008) was different, occurring at higher concentra tion in browse collected duri ng the low water season (Figure 4-4). Although mean concentration of Mn l ooks higher also during the low water season,

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68 large variation within samples yielded a non-significant test (Wilcoxont test z = 1.4, p = 0.14). Since tapirs eat leaves mainly from the Melastomaceae and Rubiaceae families, mean concentrations of minerals were comp ared among those families, pooling the other families as a third group. Differences were found only for Ca ( F2,34 = 5.3, p = 0.010) and Mg ( F 2,34 = 4.1, p = 0.024). Higher concentration of Ca was found in leaves of the Melastomaceae and Rubiaceae family, whereas Mg was more concentrated in leaves of the Rubiaceace and the other group of families. Although 14 samples of fruits were colle cted, the amount of dry pulp was enough for analyzing only 4 fruit species ( Mauritia flexousa Spondias mombin, Couma macrocarpa and Jacarantia sp.). These species, however, were among the most frequent in tapir diet (Figure 4-2), and may give a good id ea of the quality of fr uits as a source of minerals in tapirs food. When compared with browse, differences were found for 2 macrominerals (K and Na) and 2 trace elements (Mn and Fe). All these 4 elements were at higher concentrations in browse th an in fruits (Wilcoxons test: z = 3.07, p = 0.002 for K, z = 3.26, p = 0.001 for Na; z = 2.98, p = 0.003 for Mn, and t = 4.8, df = 22.9, p <0.001 for Fe). Mean concentration of Na wa s particularly low in fruits (0.03% 0.01). Since tapir mineral requirements are unknow n, concentration of minerals in tapir food was examined in relation to minimal requirements for horses (NRC 1989) because of their similarity in digestive system (Janssen et al. 1999). Levels of P were below minimal required concentrations in horse di ets (Table 4-4) in both browse and fruit samples. P levels were much below the minimal requirement for growing horses or pregnant females (Table 4-4). Although mean P le vel in browse was sli ghtly higher in the

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69 low water season, its concentration was lower than required in both seasons. Mean Na concentration in browse samples was within the minimal required for horses, but below requirements in all fruit samples (Table 4-4) Potassium levels were below requirements only in fruit samples. The remaining macrominerals were within the minimal required levels for horses, in both browse and fruit samples. Among trace elements, Zn concentration was below minimum requirements for horses in both browse and fruits, and Cu was below requirements in browse and barely at a minimum requirement in fruits (Table 4-5) However, Cu requirements for tapirs may be much higher than the requirement for horses (Janssen et al 1999), suggesting that both browse and fruits would be defi cient in Cu in tapir diet. In contrast, levels of Mg and Fe were much higher than required in horse di ets (Table 4-5). Concentration of B was similar between browse and fruit samples, but requirements have not been established in horse diets. Besides minerals, both browse and fruit samples showed high levels of crude protein (measured as N concentrations) (Table 4-5). In summary, minerals in tapir diet in the Yavari-Miri River seem adequate except for P, Na, Zn and Cu, based on requirements established for horses. Mean fecal concentration of mine rals is shown in Table 4-5. Among macrominerals, levels of P in feces were similar to those in browse and fruit. Concentration of Na in fecal samples was hi gher than the one in browse and especially fruits. Fecal concentrations of other macrominerals were always lower than concentrations in tapir foods. Most trace elemen ts where at higher concentrations in fecal samples than in tapir foods especially for Fe Zn and Cu. Fecal Fe was particularly high

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70 in fecal samples. The only exception was Mn, which was lower in feces than in browse, but was higher than in fruit samp les. No fecal B was analyzed. Discussion Lowland Tapir Diet at the Yavari-Miri Region Lowland tapir diet at the Ya vari-Miri River is composed of a large number of plant species. This result agrees with previous res earch in other tropical forests. For example, in the Tabaro River valley of Venezuela lo wland tapirs also f eed on 88 plant species (Salas 1996), and on 81 species in the Duda River of Colombia (Pea et al. 1996). Most browse samples were found in tree fall gaps or early successional stages of riverbank vegetation were plants from the Melastomataceae and Rubiaceae were growing. Those two families are typical of second growth states and are usually represented by pioneer species. Salas a nd Fuller (1996) also found such foraging behavior of lowland tapir in the Tabaro Ri ver valley (Venezuela), and established that tapirs are more selective when foraging in si tes other than tree fall gaps. In the YavariMiri River valley tapirs forage d also on growing trees with tr unks > 2 cm in diameter or semi-epiphyte plants (family Araceae) growing on tree trunks. Tapirs ate those plants mainly during their young states. Frequency of browsing on fast growing plants seems to be a characteristic of tapirs in general, accord ing to the list of brow sed species reported in the diets of the other 3 tapir species (Janzen 1982a;Terwilliger 1978; Naranjo 1995; Foerster 1998; and Tobler 2002 for Tapirus bairdii ; Downer 2001 for Tapirus pinchaque ; and Williams 1980 for Tapirus indicus ) Besides browse, fruits are very important in the tapirs diet. Th is feature was also described in the Blanco River of Peru (Bodmer 1990), French Guiana (Henry et al. 2000), Colombia (Pea et al. 1996) and Brazil (Fragoso 1997; Fragoso & Huffman

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71 2000). The most common fruits eaten by lowla nd tapirs in the Yavari-Miri River were from Mauritia palm ( Mauritia flexuosa ) and trees of Spondias mombin Couma macrocarpa and Oenocarpus bataua among others. Tapirs consume the same fruit species in other tropical fore sts and disperse many of their seeds (Olmos 1997; Fragoso 1997; Fragoso et al 2003). Overall, fruits consumed by lowland tapir in the Yavari-Miri River are very similar to t hose described for the Blanco River (Bodmer 1990), located about 100 km northwest of the Yavari-Miri ri ver, in the same continuous forest. The highest percentage of occurrence of the palm Mauritia flexousa and the occurrences of other fruit species is common in both areas. Th is resemblance is expected, since it is the same forest, and overall plant composition in both areas is probably very similar. Proportion (on a dry basis) of fruit in tapir diet in the Yavari-Miri River estimated from fecal examination seems lower than in the Blanco River, but this result does not really reflect the real proportion of fruits in the diet, since the largest seeds are not in feces. As noted by Bodmer (1990) and Henry et al. (2000) tapirs spat out the seeds of Mauritia flexuosa but large amounts of its pulp were in stomach samples. These fruits are large (about 50-60 cm long and 30-40 cm in diameter) and are covered by very small scales. Seventy percent of fecal samples fr om the Yavari-Miri valley had large amounts of Mauritia flexuosa scales. Bodmer (1990) found a simila r percentage of occurrences for Mauritia flexuosa (76.3%), examining both fecal and st omach samples. For this reason, a proportion of 33% of fruit in tapir diet (obtained from both stomach and fecal examination) in the Blanco River (Bodmer 1990) is probably a be tter estimation on the true proportion of fruit in the diet of tapirs at the Yavari-Miri Rive r. Other plant parts, such as stems, bark or wood (termed fiber in several studies) was found in tapir feces in

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72 variable amounts from about 2-68% on a dry matte r basis. This result i ndicates that tapirs feed not only on leaves and fruits. Fibrous ma terials may represent a significant portion of tapir feeding habits in some circumstances. For example, fiber content in tapir diet was very high during the low fruit producti on season in French Guiana (Henry et al. 2000). Soil also was found in 76.6% of the tapir feces analyzed, indicating that tapirs often consume soil. Since tapirs purposely visit natu ral licks (Chapter 2) soil consumption is not accidental. The amount of soil in feces was however relatively low (3.2% of fecal sample on a dry matter basis), indicating that ta pirs eat soil frequentl y, but in relatively small amounts. Soils are never discussed as part of tapir diet since this behavior has been either disregarded or considered abnormal. In fact, soil consumption is often seen as a type of pica, a behavior that refers to consumption of abnormal materials with no nutritional value (Maynard et al. 1979). Overall, tapir diet in the Yavari-Miri River is composed of a large diversity of browse, mainly from growing plants, a significant amount of fruits, mainly palm fru its, and variable amounts of fiber. Minerals in Lowland Tapir Food Animals derive the majority of their mine ral needs from their food. For herbivores, however, sources of some minerals may be limited, depending on the characteristics of the soil and vegetation. Poor mineral cont ent in vegetation may result in nutritional deficiencies if animals do not fi nd alternative mineral sources. Most minerals in lowland ta pir diets seem adequate in browse and fruits based on suggested requirements for horses, except fo r Na, P, Cu and Zn. Although mean Na in browse did not appear too low, about 50% of individual samples had Na concentration below the average. Also, Na intake from ta pir food is probably low, considering that browse accounts for only a portion of tapir food. Fruits had very low Na concentrations,

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73 and they comprise a significant part of tapir diet. Unfortunately tapir mineral requirements have not been assessed, and the assumption that their requirements are the same as horses may be inadequate for some minerals. Horses are primarily grazers feeding on high fiber diets. The digestive system of tapirs is less spec ialized than that of horses for fiber digestion (Janis 1976). Data from captive animals suggest that comparative digestibility of cellulose and hemice llulose is slightly lower in tapirs than in horses (Janssen et al 1999). Tapir fecal samples often c ontain entire leaf fragments and large fibrous materials. Coarsely chewed forages also were observed in fecal samples from the Malayan tapir in the wild (Williams 1980). These observations are in agreement with a rapid rate of food pa ssage in tapir digestive system. Efficiency of cellulose digestion reduces with an increase in rate of passage. Rate of passage in horses is lower than that of ruminants of similar weight (48 h vs 80 h) and efficiency of cellulose digestion is 70% of that of a ruminant (Janis 1976). Na re quirement in horses is higher than the requirement for ruminants (0.10% vs 0.08% respectively). Although rate of passage should not be a factor for Na, since th is element is rapidly and almost completely absorbed (McDowell 2003), the ability of tapirs to absorb Na in the lower part of the gastrointestinal track is unknown. If digesta rema ins longer in the digestive tract, it is possible that more cellulose will be broken down by microflora and thus release minerals from lignin complexes. However, this is not ex pected in tapirs, since their rate of passage seems to be very rapid. Optimal Na concentration in equine diets has been suggested to be 0.16 to 0.18% of dry matter for growth, maintenance and late gestation (Jarrige & Martin-Rooset 1981; NRC 1989). Na concentration in 51% of brow se samples and 100% of fruit samples was

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74 below the above requirements, and tapirs coul d develop a Na deficiency, especially when feeding mainly on fruits, if no other source of Na is available. Bioavailability of Na in feeds is seldom addressed because normally sodium is added to the diet as salt supplements (Ammerman et al. 1995) and it is almost completely absorbed. Bioavailability of Na in tapir food is unknow n and should be studie d. In general, most plant products have relatively small amounts of Na in comparison to animal products (McDowell 2003). Sodium (in addition to chlorine and pota ssium) is very important for maintaining osmotic pressure and regulating acid-base e quilibrium in organisms, functioning as an electrolyte in body fluids (McDowell 2003). Th ese elements are i nvolved in cellular water metabolism, nutrient intake and tran smission of nerve impulses (McDowell 2003). Sodium deficiency has been found in many tr opical locations and is one of the factors limiting animal production in some tropical countries (McDowell 1985). Tropical areas with high rainfall are usually Na-depleted since this mineral is easily leached form the soil and plants usually do not accumulate it except for halophytes(Robbins 1993). Sodium is excreted mainly in urine a nd with smaller amounts in feces. When Na intake is low the organism conserve this element by reducing its excretion (McDowell 2003). Based on the low Na concentration in ta pir food (especially in fruits) below its requirement, a potential defici ency could occur. In a defi ciency status, tapirs should reduce fecal excretion of endoge nous Na, and very little amounts of this element would be expected in tapir feces. However, fecal ex cretion of Na was not as low as expected if tapirs were facing a deficiency of this minera l. Tapirs consume soils at natural licks and those soils had higher concentration of Na as compared to non-lick soils. These results

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75 agree with the hypothesis that tapirs obtain Na from natural licks. The same could be suggested for other lick users. For example periodic Na deficiencies were suggested for frugivorous bats in a loca tion close to the Amazon a nd Napo Rivers (Studier et al. 1994), a forest relatively close to the Yavari-Miri River forest. Such a de ficiency results from low Na concentrations of fruits. Frugivorous bats were very common lick users (Chapter 2). The other macromineral that was low in tapir diet was phosphorus. Phosphorus and calcium are major mineral constituents of the animal body (Robbins 1993). In bones the ratio of Ca:P is usually constant and somewhat greater that 2:1 (McDowell 2003). Phosphorus is fundamental in almost all as pects of animal meta bolism, including energy metabolism, muscle contraction, nerve tissu e metabolism, transport of metabolites, nucleic acid structure, and nutrient meta bolism (Robbins 1993). Phosphorus absorption efficiency in horses is 35%, but it may vary according to the form (organic or inorganic) in diet, being reduced in diets with hi gh concentrations of oxalates (NRC 1989). Requirements in horses during gestation a nd lactation increase because of milk production. Calcium was at adequate levels in tapir foods, but P was significantly low. Ratios of calcium to phosphorus should be 2:1, but very low phosphorus intake is detrimental (NRC 1989). Deficiency of P produ ces rachitic changes in growing horses and osteomalacic changes in adult horses. In he rbivores, P is excreted primarily in feces, although animals fed high concentrated diet s excrete P also in urine (McDowell 2003). Levels of P in tapir feces were expected to be low since P in food was below requirements for maintenance and very low for growth and lactation. As with Na, tapirs

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76 may be adding P to their diets by consumi ng soils. Phosphorus was very high in licks soils as compared to non-lick samples. Among microminerals, Cu appears to be limiting in tapir diet. A potential deficiency of Cu could be expected from tapir diet because tapirs may have a unique metabolic requirement for this element (Janssen et al 1999). This suggestion comes from the observation that levels of Cu in 22 cap tive tapirs of 3 species had a mean serum copper level of 0.21 g/ml when a normal level in hor ses is 0.7 ppm. Dietary copper concentrations in those tapirs were ade quate in comparison to horse requirements (Janssen et al 1999). Concentration of Cu in plants depends on several factors such as form of soil copper, pH, concentration of ot her elements and organic residues and plant species. Usually, severely leached, sandy soils, alkaline soils or peat or muck soils produce plants with a low copper content. Absorption of copper tends to be low, and is affected by chemical form, copper status of th e animal and levels of other ions such as calcium, cadmium, zinc, iron, lead, silver molybdenum, and sulfur (Robbins 1993). A high proportion of ingested Cu is excreted in feces, and most fecal Cu is unabsorbed (McDowell 2003). Copper was also higher in lick soils as compared to non-lick soils (Chapter 3). By consuming those soils, tapi rs could be adding Cu to their diets. Summary and Conclusions Lowland tapirs diet in the Yavari-Miri Ri ver valley is very diverse, including more than 80 species of browsed plants and at le ast 13 species of fruits. Most browsed species are of the families Melastomataceae and Rubiaceae, and are pioneer plants growing in tree fall gaps. Fruits eaten by tapirs represent several palms and other tree species. Diet of

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77 lowland tapir in the Yavari-Miri River valley is similar to what is described for other tropical locations. Mineral contents in browse and fruits ea ten by lowland tapirs seem adequate, based on horse diets, except for Na, P, Cu and Zn, whose levels are below suggested requirements, especially for growing and lactat ing female horses. Levels of Na, P and Cu excreted in tapir feces are higher than expected if tapirs were facing a deficiency of these minerals. These elements were found in highe r concentrations in soils eaten by tapirs, suggesting that geophagy at natural licks f unctions as natural supplementation of those minerals in the forest. These results suggest that tapirs, and possibl y other lick users, obtain minerals that are in short supply in their di ets by consuming soils from natural licks. As a consequence, natural licks may be a very important res ource for lowland tapirs and possibly other herbivore/frugivore species in the Yavari-Miri River.

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78 Table 4-1. Plant species in tapir browse along the Yavari-Miri River, Peruvian Amazon. Family Species F Family Species F Anacardiaceae Spondias mombin 1 Melastomataceae Miconia nervosa 2 Annonaceae Oxandra euneura 1 Melastomataceae Miconia splendens 4 Apocynaceae Tabernaemontana flavicans 1 Melastomataceae Miconia ternatifolia *1 Apocynaceae Tabernaemontana siphilitica 1 Melastomataceae Tococa capitata 1 Araceae Anthurium brevipedunculatum 2 Melastomataceae Tococa caudata 6 Araceae Heteropsis sp. 1 Melastomataceae Tococa coronata 1 Araceae Philodendron elaphoglossoides 3 Melastomataceae Tococa guianensis 1 Araceae Philodendron rudgeanum 2 Melastomataceae Tococa setifera 1 Araliaceae Dendropanax arboreus 1 Meliaceae Trichilia pallida 1 Bignoniaceae Arrabidaea bilabiata 1 Moraceae Cecropia sp. 1 Blechnaceae Salpichlaena hookeriana 1 Moraceae Naucleopsis sp. 1 Bombacaceae Matisia bracteolosa 2 Moraceae Sorocea hirtella 1 Capparidaceae Capparis macrophylla 2 Myristicaceae Otoba glycycarpa 1 Clusiaceae Chrysochlamys sp. 1 Myristicaceae Otoba parvifolia 1 Clusiaceae Garcinia acuminata 2 Myristicaceae Virola elongata 5 Clusiaceae Moronobea coccinea 1 Myrtaceae Eugenia myrobalana 1 Combretaceae Combretum fruticosum 1 Myrtaceae Myrcia paivae 1 Combretaceae Combretum laurifolium 1 Myrtaceae Myrciaria sp. 1 Combretaceae Combretum laxum 1 Nyctaginaceae Neea floribunda 2 Convolvulaceae Maripa sp. 1 Nyctaginaceae Neea spruceana 1 Cyclanthaceae Evodianthus funifer 3 Ochnaceae Ouratea aromatica 1 Ebenaceae Diospyros poeppigiana 4 Ochnaceae Ouratea sp. 1 Ebenaceae Diospyros subrotata 1 Olacaceae Heisteria cauliflora 1 Euphorbiaceae Acalipha sp 1 Rhamnaceae Ampilozyzygium amazonicus 1 Euphorbiaceae Conceveiba rhytidocarpa 1 Rubiaceae Coussarea brevicaulis 3 Euphorbiaceae Didymocistus chrysadenius 1 Rubiaceae Faramea multiflora 3 Euphorbiaceae Mabea elata 1 Rubiaceae Psychotria capitata 1 Fabaceae Inga alba 1 Rubiaceae Psychotria cartagenensis 2 Fabaceae Inga capitata 1 Rubiaceae Psychotria cincta 1

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79 Table 4-1 (continued) Family Species F Family Species F Fabaceae Inga dumosa 1 Rubiaceae Psychotria deflexa 1 Fabaceae Inga semialata 1 Rubiaceae Psychotria iodotricha 3 Fabaceae Machaerium floribundum 1 Rubiaceae Psychotria loretensis 1 Fabaceae Macrolobium angustifolium 1 Rubiaceae Psychotria lupulina 1 Flacourtiaceae Hasseltia floribunda 1 Rubiaceae Psychotria p oeppigiana 2 Flacourtiaceae Ryania speciosa 1 Rubiaceae Psychotria tenicaulis 5 Flacourtiaceae Tetrathylacium macrophyllum 1 Rubiaceae Warszewiczia coccinea 1 Hippocrataceae Salacia sp. 1 Sapotaceae Micropholis egensis 1 Icacinaceae Humirianthera ampla 1 Sapotaceae Pouteria guianensis *4 Lecythidaceae Eschweilera tessmannii 1 Solanaceae Cestrum microcalyx 1 Melastomataceae Coussarea brevicaulis 1 Solanaceae Cestrum sp. 1 Melastomataceae Henriettea lasiostylis 3 Solanaceae Solanum sp. 1 Melastomataceae Loreya mespiloides 1 Violaceae Leonia glycycarpa 1 Melastomataceae Miconia amazonica 1 Vochysiaceae Vochysia lanceolata 1 Melastomataceae Miconia eriocalyx 1 Vochysiaceae Vochysia lomatophylla 3 Melastomataceae Miconia mazanana 1 Non-identified 1 F = Frequency of each plant species in tapir browse samples. = Samples analyzed for N and mineral (P, K, Ca, Mg, S, Na, Mn, Zn, Cu, Fe, B) content.

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80 Table 4-2. Number of composite sample s of each family analyzed for mineral concentrations in 2 seasons in the Yavari-Miri River valley, Peruvian Amazon. Season Family High water Low water Araceae 0 1 Araliaceae 0 1 Bignoniaceae 0 1 Clusiaceae 0 2 Combretaceae 0 1 Euphorbiaceae 0 1 Fabaceae 0 2 Flacourticeae 1 0 Hippocrataceae 1 0 Melastomataceae 1 8 Moraceae 1 0 Myristicaceae 1 1 Myrtacea 3 0 Nyctaginaceae 0 2 Myrtaceae 0 0 Rubiaceae 2 3 Sapotaceae 0 2 Vochysiaceae 0 1 Non-identified 1 0 Total samples 11 26

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81 Table 4-3. Fruits in lowland tapir diet in the Yavari-Miri River valley, northeastern Peruvian Amazon. Evidence Family Species Local name Feces Feeding sign Anacardiaceae Spondias mombin Uvos X X Annonaceae Annona sp. Sacha anona X X Apocynaceae Couma macrocarpa Leche caspi X X Arecaceae Mauritia flexuosa Aguaje X X Arecaceae Oenocarpus bataua Hungurahui X Arecaceae Attalea sp. Shebon X Caricaceae Jacarantia sp.* Papaiya X X Cecropiaceae Pourouma sp. Sacha uvilla X Celastraceae Maytenus sp. Sacha shushuhuashi X Chrysobalanaceae Licania sp. Parinari de altura X Fabaceae Hymenaea sp. Azucar huayo X Moraceae Ficus insipida Oje X Sapotaceae Pouteria sp. Sacha caimito X Fruits analyzed for N and mineral (P, K, Ca, Mg, S, Na, Mn, Zn, Cu, Fe, B) content.

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82 Table 4.4. Mean content of nitrogen and m acrominerals in tapir foods (browse and fruits), suggested requirements (based on guidelines for horses) and mean concentrations of excreted N and macrominerals in tapir feces. N P K Ca Mg S Na % dry matter Tapir food Browse Mean 3.44 0.12 0.73 0.53 0.27 0.15 0.22 SD 1.13 0.05 1.26 0.32 0.14 0.03 0.13 Fruits Mean 1.20 0.11 0.14 0.70 0.14 0.36 0.03 SD 0.80 0.08 0.03 0.94 0.13 0.34 0.01 Required1 Maintenance 0.17 0.30 0.24 0.09 0.15 0.10 Growth 0.17 0.380.30 0.31 0.680.10 0.15 0.10 Females2 0.34 0.38 0.45 0.10 0.15 0.10 Tapir feces Mean 2.38 0.14 0.18 0.26 0.12 0.09 0.29 SD 0.65 0.09 0.18 0.21 0.7 0.05 0.25 SD = 1 Standard deviation. 1 Suggested requirements based on gu idelines for horses (NRC 1989). 2 Suggested requirements for pregnant and lactating females based on guidelines for horses (NRC 1989).

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83 Table 4-5. Mean content of microminerals in tapir foods (browse and fruits), suggested requirement (based on guidelines for horses) and mean concentrations of excreted microminerals in tapir feces. Mn Zn Cu* Fe B mg-kg-1 Tapir food Browse Mean 454.49 32.30 7.15 348.94 14.91 SD 471.61 39.36 6.46 290.34 9.87 Fruits Mean 42.98 22.45 10.55 70.48 14.33 SD 52.89 7.39 5.56 62.44 0.65 Required1 Maintenance 40.00 40.00 10.00 40.00 Growth 40.00 40.00 10.00 50.00 Unknown Females2 40.00 40.00 10.00 50.00 Tapir feces Mean 202.04 85.54 42.86 2952.15 SD 151.34 91.12 68.25 11767.28 1 Suggested requirements for horses (NRC 1989). 2 Suggested requirements for pregna nt and lactating females (NRC 1989). Copper requirements for tapirs may be much higher than requirement for horses (Janssen et al. 1999).

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84 Figure 4-1. Percent distribution of plant families browsed by lowland tapir ( Tapirus terrestris ) in the Yavari-Miri River valley, of the northeastern Peruvian Amazon 01020304050607080Pouteria sp. Pourouma sp. Licania sp. Hymenaea sp. Maytenus sp. Jacarantia sp. Attalea sp. Couma macrocarpa Oenocarpus bataua Spondias mombin Annona sp. Mauritia flexuosa % of occurrence in tapir feces Figure 4-2. Percentage of occurrence of seve ral fruit species in lo wland tapir feces along the Yavari-Miri River valley, Peruvian Amazon.

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85 0 0.2 0.4 0.6 0.8 1 1.2 PKCaMgSNaConcentration (% dry basis) High water season Low water season Figure 4-3. Concentration of macrominerals in tapir browse, duri ng high water and low water seasons in the Yavari-Miri Rivi er valley, Peruvian Amazon. Vertical lines indicate 1 standard deviation. 0 100 200 300 400 500 600 700 MnZnCuFeBConcentration (mg-kg-1) High water season Low water season Figure 4-4. Concentration of trace minerals in tapir browse during high water and low water seasons in the Yavari-Miri Rive r valley, Peruvian Amazon. Vertical lines indicate 1 standard deviation.

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86 CHAPTER 5 NATURAL LICKS AND RURAL PEOPLE OF THE AMAZON Introduction For most rural communities of the Amazon, wildlife hunting conti nues to be one of the most important sources of subsistence (Alvard et al 1996; Robinson & Bodmer 1999). Although most hunting is primarily for s ubsistence, over-harvest ing is associated with current declines of many wildlife populations. A large body of research exists on the effects of subsistence hunting on wildlife popul ations and its sustainability (examples in Robinson & Redford 1991; Bissonette & Kr ausman 1995; Robinson & Bennett 2000). Non-sustainable harvest rates have been f ound in many studies for a number of species. Besides the effects on wildlife, over-harves ting threatens food security of communities that rely on game for their subsistence. Clear ly, wise wildlife manage ment is needed in order to secure both human well-being and wildlife persistence in tropical regions. Appropriate wildlife management in the Amazon requires an understanding of the hunting systems in the region and the elements that may represent important components of the system. Hunting systems vary depending on the attributes of the environment and ethnic composition of communities (Redfo rd & Robinson 1987; Bennett and Robinson 2000). An often overlooked characteristic feat ure of western Amazon is the existence of natural licks that provide nutri tional benefits to wildlife (Cha pters 3 and 4). Natural licks attract a number of species a nd become sites of either high congregation of animals, or a natural trap for a solitary animal. Such a feature has been observed in other tropical regions where hunters take good advantage of the animals need for the licks

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87 (Seidensticker & McNeely 1975). In many areas of Amazonia, the existence of licks represents an important criterion for a person to establish a hunting site (Puertas 1999). This corresponds to the common practice of many hunters of waiting for game animals at natural licks, especially during the dry s eason (Ayres & Ayres, 1979). Accounts of the use of natural licks as hunting sites seldom app ear in the literature, and therefore little is known of the relative importance of these places in terms of their contribution to overall hunting in an area. A study in an indigenous community in Colombian Amazonia revealed that 25% of the m eat consumed was obtained from natural licks (Walshburger & Hildebrand 1988). Indigenous cultures of west ern Amazonia apparently prevented overharvesting of wildlife at natural licks by a set of cultural practices and beliefs. For example, the Uitoto Indians regard natura l licks as dangerous and mysterious places, where hunting is allowed only under a set of cultural prescriptions (Pineda 1992). Because such prescriptions are uncomm on within many human communities in the Amazon, hunting at licks is usually uncontrolled. The purpose of this chapter is to examine the importance of natural licks in subsistence hunting in an Amazonian rura l community and its implications for management and conservation. This is done by (1) examining the relative contribution of natural licks to the overall hunting, (2) inve ntorying, locating and describing the licks used as hunting sites, and (3) examining hunters perceptions a nd beliefs concerning natural licks. The main hypotheses examined in this chapter are the following: Hypothesis 1 Hunting at natural licks provi des a higher contribution to the overall harvest, at least for some speci es, as compared to other hunting sites Hypothesis 2 Most hunters use natural licks as hunting sites.

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88 As a framework to understand the manageme nt and conservation implications of this study, background information about the community and the current wildlife comanagement process going on in the area is presented first. Study Area Location and Biophysical Setting This study was conducted at Nueva Espera nzaVillage, a small rural community located at 4o19 S, 71o 57 in the low Yavar-Mir River region in northeastern Peruvian Amazon (see description below). The landscape is dominated by continuous tropical rainforest dissected by the Yavari-Miri River and its tributaries such as Arabela, Esperanza and Panguana Creeks. Types of fo rest in the area include upland forest on terraces and sedimentary planes and flooded fo rest in relatively narrow flood planes of the Yavari-Miri River and its tributaries. Mean annual temperature is 26oC, with monthly mean maximum temperatures ranging from 28-30oC, and monthly mean minimum from 17-20oC. Mean annual precipitation ranges fr om 2400 to 3100 mm (Marengo 1998), with the highest monthly rainfall occurring from Febr uary to April, and the lowest from June to September. Plant and animal diversity is high in the area. Estimated regional species richness includes up to 3,500 plants (Pitman et al. 2003), 393 fishes (Ortega et al 2003), 123 amphibians and reptiles (Rodrig uez & Knell 2003), 550 birds (Lane et al 2003) and over 80 mammalian species (Valqui 1999; Salovaara et al 2003). History and Description of Nueva Esperanza Village Like most of the Amazon region, the Yava ri and Yavari-Miri Rivers have an interesting history of consecutive raises and falls of economic booms including rubber, timber, rosewood oil, and animal pelt extract ion, with resulting fl uctuations in human population demographics (a more detailed acc ount in Bodmer & Puertas 2003). Prior to

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89 the beginning of the rubber boom (in the late 1800s) the human inhab itants of the YavariMiri region were mainly native communitie s of Matses Indians (known also as Mayurunas), whose territory included the whol e Yavari valley. But with the intermittent economic activities, the Yavari region b ecame more populated, and many non-indigenous settlements were established along the rivers By the 1960s more than 1000 people were living along the Yavari-Miri Ri ver (Bodmer & Puertas 2003). However, a progressive decline in economic activities in the area since the 1970s and a high incidence of malaria (with a deadly epidemic outbr eak in 1995) resulted in the reduction of human population. Almost half of the population died and most of the survivors migrat ed to other areas. Currently, the Yavari-Miri River is probably at its lowest human population density since the beginning of the rubber boom (Bodmer & Puertas 2003). Currently, the only 4 small communities along the Yavari-Miri River are: Carolina, in the lower course of river, Nueva Espera nza and San Felipe close to Esperanza Creek (Figure 5-1), and San Francisco de las Mercedes comprised of only one family in Pavaico Creek, in the upper part of the Yavari-Miri Ri ver. Nueva Esperanza v illage is the largest of the 4 communities. It was founded in 1971 (Bodmer & Puertas 2003) and according to the oldest settlers, it was first established close to the mouth of the Esperanza Creek. However, repeated flooding motivated settle rs to move the community to its current location, on a high terrace around 18 km downstream As in other rivers of the Peruvian Amazon, inhabitants of the Yavari-Miri River are ribereos detribalized communities of several origins (Bodmer 1994). According to a census conduc ted in year 2002 (Montenegro unpublished data), the oldest members of Nueva Esperanza came from

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90 several areas of the Amazon River and its tributaries (I quitos, Pebas, Tamshiyacu, Cochiquina, Rio Tigre, and Nauta). In 2002, Nueva Esperanza village had 162 i nhabitants, grouped in 28 households Average size per of household was 6, with a hi gh proportion of infa nts (Figure 5-2). The village has a primary school (with intermittent absence of a teacher), and an infirmary for first aid services. The closest hospital is on the Yavari River, in a Brazilian military base at the international border betw een Peru and Brazil. It take s 1 day to travel from the community to the hospital paddling in a canoe The main subsistence activities in Nueva Esperanza village are wildlif e hunting, fishing, agriculture and low scale extraction of trees for fruits or wood (Antunez 2001; Del Campo et al 2003). There is an average of 1 hunter per family. Hunting in the Yavari-Miri Ri ver is slight compared to other areas in northeastern Peru, and this ar ea still maintains abundant w ildlife populations. Currently the Yavari-Miri basin is the most important area for wildlife recovery from hunted areas of the Orosa, Maniti, Tamshiyacu, Tahua yo, Yarapa, Galves and Yaquirana (Bodmer et al 2003). To the northwest of Nueva Esperanza, in the headwaters of the Yavari-Miri River, lies the Reserva Comunal Tamshiyacu-Tahua yo (RCTT). This reserve covers 322,500 ha, that also includes the upper Tamshiyacu and Tahuayo river watersheds. The RCTT was created in 1991 by the Department of Loretos government, in response to a joint effort of local communities and researchers (Meyer & Penn 2003). The RCTT is run by the local communities of the Tamshiyacu and Tahuayo Rivers, and comprises areas of use for managed hunting and extraction of other natura l resources, and areas of strict protection. Local hunters work together with extensi on workers and researchers monitoring hunting

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91 levels (Puertas 1999, Bodmer & Puertas 1999, Meyer & Penn 2003). Although the 4 communities of the Yavari-Miri River are located outside the reserve, they have participated in the wildlife co-managemen t initiative since 1994, primarily in selfmonitoring of hunting levels. Currently, several threats to local lifestyl e practices exist in the region (Del Campo et al 2003): medium-and large s cale logging prospects, immigr ation of outsiders with agricultural practices incompatible with local natural resources, and irregular provision of basic services. Settlers of Nueva Espera nza are currently concerned about the reemergence of large-scale extractive activities and high-impact agri cultural practices of colonists. Immigrant members of a religious sect (colloqui ally referred as to the Israelitas) are already settled in the lowe r Yavari River, and plan to extend their territories towards less inhabited areas. An im mediate goal of settlers of Nueva Esperanza is to acquire legal title to their lands and government recogn ition of a protection area for the region (Del Campo et al 2003). In summary, Nueva Es peranza village is a small ribereo community living in the area for more than 40 years, curre ntly practicing low impact resource use, and activel y involved in the management of their natural resources. Methods Subsistence Hunting Records This study was linked to the community based co-management process going on in northern Peru (Puertas 1999; Bodmer & Puertas 1999; Bodmer et al 2003), which includes a permanent hunting register by rural hunters in the Yavari -Miri area. Hunting records have been kept in Nueva Esperan za village since 1994 (Puertas 1999). Since 2001, hunting records included not on ly the species and hunting ar ea, but also the specific hunting site (natural lick, fo rest, and riverbank). Hunting records from January to

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92 December 2001 were used in this researc h. Species hunted, number of animals and biomass were compared among hunting sites (natur al licks, forest trails and riverbanks). Natural Lick Mapping and Description Most licks used by hunters of Nueva Esperanza were visited in 2002, guided by the most experienced hunters of the village. Li ck locations were obtained from a global positioning system (GPS), and access trails a nd other features were drawn with the hunters help. Also, size of licks was obtaine d by measuring both its length and width. Lick boundaries were determined as the limits where animal activity was evident. Animal tracks at the licks were recorded, and addi tional information of lick users was obtained from the hunters. Skull and other bones, as well as platforms or other evidence of hunting at the licks were recorded. Licks were located on a map (1:100,000 scale) to estimate the distance traveled from the comm unity to the licks, and the overall spatial layout of the licks. When possible, location of other hunting sites was also included on the map. Location of hunting trails was obt ained combining both hunting registers and geographical information on streams, lakes and other features collected during the mapping process. From information provide d by hunters, buffer areas of 5 km around hunting trails were calculated using the ArcV iew software (version 3.2) to visualize the area of harvesting. Natu ral licks used by hunters were ove rlaid on top of the calculated buffer areas to visualize their location in re lation to the hunting area. Both hunting areas and licks were displayed on top of a satellite image of the area. Hunters Perceptions Concerning Natural Licks Structured interviews were conducted w ith the 27 hunters at Nueva Esperanza. Interviews addressed the following subjects: (1 ) preferred hunted si tes, (2) perceptions about natural licks, including types of licks, descriptions and drawi ngs, (3) species hunted

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93 at licks, (4) hunting technique s at licks, (5) beliefs con cerning licks, and (6) lick management including conservati on perceptions and attitudes. Results Subsistence Hunting in Nueva Esperanza Village Hunting records indicate that 683 animals from 19 species were harvested from January to December 2001 (Table 5-1). Game species included 1 species of Amazonian tortoise ( Geochelone denticulata ), at least 5 species of large birds form the families Cracidae (2 species) and Tinamidae (1 species ), and 13 species of mammals, including 1 carnivore species ( Nasua nasua ), 5 species of medium and large primates ( Alouatta seniculus Ateles paniscus, Cebus albifrons, and Lagothrix lagothricha and Pithecia monachus ), all ungulates na tive to the area ( Tapirus terrestris, Tayassu pecari Pecari tajacu Mazama americana and M. gouazoubira ) and 2 large rodents ( Agouti paca and Dasyprocta fuliginosa ). Harvest was not evenly distributed am ong species (Figure 5-3). White-lipped peccaries ( Tayassu pecari ) and collared peccaries ( Pecari tajacu ) were the most frequent prey animals, accounting for 55% and 22% of the total number of harvested animals respectively. Lowland tapirs ( Tapirus terrestris ) were the next most frequent prey species, accounting for 8% of th e total number of hunted animals. Red brocket deer and large primates represented about 4% each of the total harvested individuals. The remaining species accounted for 0.1% to 3% of the total number of harvested animals. Total biomass hunted during year 2001 wa s 26, 211 kg. Contribution of each game species to the total harvested biomass diffe red among species (Figure 5-4). White-lipped peccaries contributed to the 47.5% of the tota l harvested biomass. Lowland tapirs made up 33% of total biomass, followed by collared peccaries, representing 14.2%, and red

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94 brocket deer representing 3.7%. The remain ing species contribution to total biomass ranged from 0.1% to 0.9%. There were differences in total biomass obtained from each hunting site. Hunting along trails provided 65% of the harvested biom ass, whereas natural licks and riverbanks provided 18% and 17%, respectively (Figure 5-5). Most white-lipped peccaries were obtained along hunting trails (F igure 5-6), and in less propo rtion at natural licks and riverbanks. In contrast, lowland tapirs were hunted mainly at natural licks and riverbanks, and to a lesser extent alo ng trails. Collared peccary and red brocket deer were hunted along trails, and occasionally in natural licks. Natural Lick Mapping and Description Hunters of Nueva Esperanza village use more than 42 natural licks as hunting sites. These licks are located along the Esperanza Creek (20 licks) and the middle and low Yavari-Miri River (22 licks). Mo st licks used as hunting site s are located at or near the riverbanks in both the Yavari-Miri River a nd the Esperanza Creek (Figure 5-7). Only 6 licks (14%) were located more than 500 m fr om the riverbank, up to 1 km inside the forest. Size of natural licks varied from 110 m2 to 1,200 m2. All hunted licks were found within the 5 km buffer areas from hunting tr ails. Distance from Nueva Esperanza village to the licks varied from 10 to 35 km (strai ght line), but travel times vary throughout the year according to river levels. Remains of rustic temporary platforms built by hunters were found in 5 licks. These platforms allow hunters to wait for game animals at the licks. For many of the riverbank licks, waiti ng for animals is done from a canoe, instead of a platform. Another alternat ive is using a hammock instead of a platform, in order to hunt inside a lick. Bones of lowland tapirs (mainly skulls) were found near 2 natural

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95 licks. Hunters report that they usually do not process their k ill inside the licks, and that bone and other materials are not left close to the licks. Several hunter camps were found close to a number of natural licks. Hunters indicated that occasiona lly they conduct hunting trips of 5 to 10 days when they desire to hunt in those areas far away from the commun ity. Usually they maintain a campsite close to licks and surrounded by hunting trails. Hunters Perceptions Concerning Natural Licks All hunters of Nueva Esperanza were in terviewed in order to gather their perceptions about natu ral licks. Most hunter s listed all ungulates, large primates, large rodents and large birds as pot ential prey at natural lick s. However, there were only ungulates reported as prey in natural licks in 2002. Most hunters recognized more than one type of natural lick, depending on either the species using them or their location. Hunters classification of natu ral licks included the following: tapir licks, deer licks, peccary licks and small animal licks. Differences among those licks are mainly in size, with the tapir licks being the largest. Most hunters (75%) indi cated that large natural licks are more frequent in a type of upland forest named shapajillal This type of forest is characterized by the dominance of shapaja a palm of the genus Attalea However, most hunters also recognized that many licks they use are those close to the river, in seasonally flooded forest or along riverbanks. About 70% of hunters of Nueva Esperanza village expressed th eir preference for using licks as hunting sites, whereas 30% of them stated that they dislike hunting at licks. The former group indicated that natural licks are a very reliab le site for hunting lowland tapirs, and occasionally other species. The la tter group stated that even though they could hunt tapirs, nocturnal waiti ng at the licks is very unpl easant, and even dangerous.

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96 Almost all hunters (90%) have beliefs rega rding mythical owners of natural licks. However, only a few (2%) claim having actual experiences that reinforce those beliefs. For 96% of interviewed hunters, some natural li cks have a mother that may interfere or even prevent hunting at licks. The practical resu lt of those beliefs is that hunters use only those licks where they believe the mothe r does not exist or is not dangerous. About 74% of hunters of Nueva Espera nza village proposed that the best management strategy to avoid over-exploitation of natural lic ks is rotation of their use through time. About 21% of hunters indicated th at prey should not be processed at the licks to avoid degradation of animal remains that ma y damage the licks, as a management strategy. Finally, 5% of hunters stated that management of licks should involve exclusion of alien hunt ers coming form outside area s, in order to avoid overexploitation of natural licks. Discussion Subsistence Hunting Records From the hunting records in Nueva Esperan za village, it is clear that subsistence hunting in the Yavari-Miri Rive r is concentrated in large mammals, especially ungulates. The most frequently harvested mammals are white-lipped peccary and collared peccary, and to a lesser extent the lowland tapir. However, when compari ng the contribution of each species to the total harv ested biomass, lowland tapirs are second after white-lipped peccaries, accounting for about 33% of total bi omass. Peccaries are harvested with more frequency along hunting trails, whereas the lowland tapir is harvested with more frequency at natural licks and riverbanks. A close examinati on of tapir hunting records by month indicated that tapirs were harvested inside natural licks on average 68.66% of the occasions, except in November, when more ta pirs were harvested at the riverbanks.

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97 Examination of riverbank locations wher e tapirs were hunted in November 2001 indicated that 3 of the 7 hunti ng sites were very close to natural licks (sites Gamarra, Guedes and Maquisapay). In other words, mo st of the lowland tapir hunting occurred inside or around natural licks. Total biomass from lowland tapirs harves ted inside and around natural licks adds up to 25% of total biomass hunted in the Yavari-Miri River in 2001. The other species harvested at licks provide an additional 10% of the total biomass, for a total of 35% of biomass obtained from licks. The effect of hunting at licks varies am ong species. Peccaries are hunted at licks but less extensively than tapirs Hunting of peccaries could be sustainable, within certain limits (Bodmer et al 1997a). In contrast, lowland tapi rs are more susceptible to overhunting than other Amazonian species because of their low reproduction rate, long generation time and longevity (Bodmer et al 1997b). Tapirs visit li cks in a predictable manner, making them more suscepti ble to hunting at those sites. A preliminary analysis of hunting at lic ks in the same area showed the same tendency, with most tapirs hunted at natu ral licks (Parish 2001). Proportion of hunted animals at licks was higher for all ungulates in terms of biomass during April-June 2001 (Parish 2001). Although proportions differ a littl e when using data for the whole year, similar patterns were seen. Compared to hunting at Quebrada Blan co, another location inside the RCTT, hunting pressure in the Yavari -Miri region is lower. Huntin g at Quebrada Blanco is 5 times greater than at the Yavari-Miri River, and most large mammal species are harvested above sustainable levels (Bodmer et al 2003). Recent analysis of capture for unit effort

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98 in both the Yavari-Miri River and Quebrada Blanco (Bodmer et al 2003) indicated that lowland tapir in the Yavari-Miri River is curr ently hunted within sustainable levels with 16% of its reproductive productiv ity being harvested. In contra st, lowland tapir is clearly over-harvested at Quebrada Blanco, where 140% of tapir reproductive productivity is taken (Bodmer et al 2003). Natural licks are frequently used in Quebrada Blanco, and are in fact an essential requirement for a hunt er to establish a hunti ng site there (Puertas 1999). The larger human population size of Queb rada Blanco compared to the YavariMiri River site accounts for differences in hunt ing pressure between the 2 sites. In order to maintain lowland tapir hunting within sust ainable levels, it is important to consider their high susceptibility at licks, and to regulate harvest from licks as a part of the wildlife management in the Yavari-Miri River. Such a management strategy is very important, since the Yavari-Miri River vall ey is currently considered as a source area (on a sourcesink model) for other heavily hunted areas of the northern Peruvian Amazon (Bodmer et al 2003). For the Yavari-Miri region to eff ectively work as a source, its populations should be near carrying capacity (Pulliman 1988) so animal dispersal can replenish the hunted (or sink) areas. Such a system is ve ry important for sustainability of wildlife hunting in Amazon (Sirn et at 2003), and particularly fo r lowland tapirs (Novaro et al 1999, Salas & Kim 2002). Natural Lick Mapping and Description Local hunters at the Yavari-Miri River use a relatively large number of licks. The 42 licks inventoried in this re search comprise 82% of the total number of natural licks (52) used in the area (Parish 2001). The addi tional 10 licks are loca ted in the upper part of the Yavari-Miri River, and are used only occasionally. From hunting records, the most used natural licks are those located along th e Esperanza Creek, and some of the licks

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99 located along the Yavari-Miri River within 30 km from Nueva Esperanza village. Parish (2001), using a participatory mapping approac h, and interviews of 12 hunters of Nueva Esperanza, found that hunting pressure was gr eater at those licks more accessible to the community. Similar results were found in this study. Also, licks loca ted within the first 500 m from the river are more frequently use d. Hunters avoid using distant licks because carrying the kill would be difficult, especially when a 250-kg tapir is the prey. This fact allows animals to switch to licks that are less visited by hunters. However, during the low water season, many small streams dry up and animals are forced to approach the riverbanks. During those mont hs, hunting at riverbank li cks becomes more common. For the above reason, management of hunting at natural licks should take into account changes in natural lick temporal availability and spatial layout. Hunters’ Perceptions Concerning Natural Licks Although Nueva Esperanza village is a ribereo community, where their members do not identify themselves as indigenous peopl e, interviews showed that some of the original indigenous beliefs are still present in the ribereo culture. For example, beliefs concerning the “mother” of natural licks are al so present in several Indian cultures of the Colombian Amazon (Pineda 1992). In the past those beliefs probably functioned as an intuitive management practice that avoided over-exploitation of wild life at natural licks. Among the Uitoto Indians of Colombia, for instance, natural licks are considered dangerous and mysterious places where the “mother of the lick” does not facilitate hunting unless the hunter follows a set of cultural prescription s. Disease or misfortune that happens after treating natu ral licks barbarously would be interpreted as a punishment (Pineda 1992).

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100 Although beliefs concerning na tural licks are not exactl y the same in the Nueva Esperanza village, hunting at licks is still asso ciated with mythical owners. The extent to which those beliefs currently function as an intuitive mana gement practice is not very clear. Hunters’ preference for or avoidance of natural licks as hunting sites seems related to individual experiences and hunting expert ise. Some hunters seem to specialize in peccary hunting, whereas others are less select ive of their prey. Those hunters claiming previous negative experiences at natural licks are less willing to spe nd night hours at licks waiting for tapirs. In contrast, many other hunters decide where to hunt depending on time, logistics and prey demand. Although hunt ing at the Nueva Esperanza village is mainly for subsistence, part of the kill is often sold or exchanged for other food products with 1 or 2 members of the community. The latter, take the meat, as well as other products, to the closest town, Islandia, close to the Yavari River’s mouth in the Amazon River. Occasionally tapir meat is in mo re demand in Islandia and other towns, encouraging settlers of Nueva Esperanza v illage to increase their hunting of tapirs. During these times hunting at natura l licks may become very common. Natural licks also are used indirectly to track other species. For example, during the interviews several hunters indicated that they could monitor white-lipped peccaries’ movements and herd size by checking tracks at natural licks. Hunters can estimate the time when white-lipped peccaries had passed thr ough the licks, and if vi sits were recent, hunters could follow peccary tracks to find the herd. In general, natural licks are an important resource for local hunters because they directly provide a significant portion of the hunted biomass, highly represented by lowland tapirs, and indirectly help to monitor other game species. All hunters interviewed

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101 were receptive to a management strategy that allows protection of the licks. The most frequent strategy mentioned by the hunters wa s rotation of hunting at natural licks. Such a strategy coincides with one of the recommendations for wildlife management for the RCTT described by Puertas (1999), who also proposed a zoning of th e area that allows rotation in natural resource us e. The mapping of all licks us ed by hunters could be used as a starting point to design a rotational sy stem for controlling over-hunting at natural licks. Also, the existence of natural licks in an area should be a criterion in delimiting protected areas. Summary and Conclusions The purpose of this chapter was to analyze the importance of natural licks for rural people of the Amazon. For the study, hunti ng patterns at the community of Nueva Esperanza along the Yavari-Miri River were analyzed through three complementary methods. First, an analysis of one-year-long hunting registers was c onducted in order to evaluate the proportion of harvest coming from licks as compared to other hunting sites. Lowland tapirs provided over 30% of tota l biomass hunted during 2001, and they were mainly hunted at natural licks and surrounding areas. Second, inventory of licks showed that hunters of Nueva Esperanza village use more than 40 natural licks located along the Esperanza Creek and the middle and low Yavari -Miri River. Most licks used as hunting sites are located close to the river, to f acilitate carrying of prey. Third, interviews conducted with all hunters at Nueva Esperanza village showed that cultural beliefs are still present in this ribereo community, and that most hunters are receptive to management strategies for controlling over-hunt ing at natural licks, mainly by rotation of use.

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102 Results of this research i ndicate that natural licks are a very important resource for local hunters because they provide direct a nd indirect hunting benef its. Natural licks are the main source of the largest mammal of the Amazon, the lowland tapir. Indirectly, natural licks provide, besides a portion of the harvest, a source of information about the most hunted species in the area, the white -lipped peccary. A management strategy that involves protection of licks and rotation of th eir use was stated as the most recommended practice in the area.

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103 Table 5-1. Species hunted by settlers of Nu eva Esperanza Village in the Yavari-Miri River from January to December 2001. Species English name Local name Number hunted in year 2001 Biomass per individual (Kg) Reptiles Testudines Family Testudinae Geochelone denticulata Amazonian tortoise Motelo 21 5 Birds Craciformes Family Cracidae Crax spp and Mitu spp Curassows Paujil 15 3 Penelope jacquacu Spix's guan Pucacunga 3 3 Pipile cumanensis Blue-throated Piping-guan Pava negra 1 3 Tinamiformes Family Tinamidae Tinamus sp. Tinamu Perdiz 1 3 Mammals Carnivora Family Procyonidae Nasua nasua South American coati Achuni 1 4 Primates Family Cebidae Alouatta seniculus Red-howler monkey Coto 8 Ateles paniscus Black spider monkey Maquisapa 2 11 Cebus albifrons White capuchin monkey Mono blanco 1 3 Lagothrix lagothricha Wooly monkey Choro 22 8 Pithecia monachus Black saky monkey Huapo negro 1 2 Perissodactyla Tapirus terrestris Lowland tapir Sachavaca 54 160

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104 Table 5-1 (continued) Species English name Local name Number hunted in year 2001 Biomass (Kg) Artiodactyla Family Tayassuidae Tayassu pecari White-lipped peccary Huangana 377 33 Pecari tajacu Collared peccary Sajino 149 25 Family Cervidae Mazama americana Red-brocket deer Venado rojo29 33 Mazama gouazoubira Grey-brocket deer Venado gris1 15 Rodentia Family Agoutidae Agouti paca Paca Majs 3 5 Family Dasyproctidae Dasyprocta fuliginosa Black agouti Auje 2 5 Total hunted in year 2001 683 26,211

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105 Figure 5-1. Location of the study area in the Yavari-Mir i River region, northeastern Peruvian Amazon.

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106 0 10 20 30 4 0-10 11-20 21-30 31-40 41-50 51-60 > 60 40 2002040 Women Men Figure 5-2. Gender and age composition of Nu eva Esperanza Village in the Yavari-Miri River region, northeastern Peruvian Amazon (census conducted in 2002). Numbers to the left indicate age class. Figure 5-3. Percent contribution of each species to the total number of animals hunted in 2001 in the Yavari-Miri River.

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107 Figure 5-4. Percent contribution of each spec ies to the total biomass hunted in 2001 in the Yavari-Miri River.

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108 Figure 5-5. Proportion of biomass harvested by hunters of the Nueva Esperanza Village per hunting site from January to December 2001. Figure 5-6. Biomass hunted per ungulate species at riverbanks, natural licks and hunting trails in the Yavari-Miri River region during year 2001.

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109 Figure 5-7. Location of hunti ng areas and natural licks used by settlers of Nueva Esperanza village.

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110 CHAPTER 6 SYNTHESIS AND CONCLUSIONS This research addressed the importance of natural licks fo r both wildlife and humans in the Yavari-Miri valley in northeas tern Peruvian Amazon. A keystone role is attributed to natural licks to both wildlife and people in th is particular region, western Amazonia. This synthesis examines the extent to which a keystone ro le can be credited to natural licks based on the results of this research. The following predictions were stated in th e introduction of this dissertation: (1) a high proportion of wildlife species use the lick s, (2) natural licks provide something to their users that is in short supply and is not easily substitutable (low redundancy), (3) natural licks are a reliable resource (are ava ilable when the animals need them), and (4) area occupied by natural licks in the habitat is small relative to its effect on its users. We found that a relatively large number of species use the licks, mainly large birds and mammals (Chapter 2). Among mammals, all ungulate species, 2 of 3 species of large primates, 2 of 3 large rodents, and many fru it bats were frequent lick users. Even 2 carnivores were found visiting li cks, possibly looking for pre y. These results agree with the prediction of a high proportion of speci es using natural licks as a resource. Examination of the chemical composition of soils consumed by wildlife species at natural licks indicates that several elements of nutritional importance (Na, Ca, Mg, P, Cu, S and B) are in relatively high concentra tions thought the year (Chapter 3). The hypothesis that some of these elements are in short supply in animal diets was tested for the most frequent lick visitor, the lowland ta pir (Chapter 2), by examining its diet and the

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111 mineral composition of its foods (Chapter 4) We found that tapir foods are good sources of mineral nutrients, except for Na, P and Cu, as compared to mineral requirements. Since tapir mineral requirements are unknow n, the assumption was made that their requirements are similar to those in horses, although the adequacy of such assumption is discussed (Chapter 4). Also, it was found that fecal mineral excretion of those elements was higher than expected considering their low concentration in foods, suggesting that tapirs are supplementing their diets by consumin g mineral-rich soils at natural licks. This idea is supported by the fact th at over 76% of the tapir fecal samples examined contained visually noticeable amounts of soil. Na wa s particularly low in fruits consumed by lowland tapirs. Whether that feature is common to most fruits in the area needs to be investigated. However, if that is the case, Na from licks is probably also of benefit for other lick users, since many of them were fr ugivore species (Chapt er 2). Results from Chapters 3 and 4 agree with the prediction th at natural licks provide something to its users that is in short supply (at least for ta pirs), and is not eas ily substitutable (low redundancy). Reliability of natural licks as a source of minerals could be inferred from Chapter 2. No significant drops in mineral content of consumed soils were found throughout the year, indicating that natural licks are a reliab le resource for the animals. However, not all natural licks are available year-round, since the ones located along the riverbank and in low plains become flooded during the high water season. Fo r this reason, natural licks located in the upland forest are more reliab le through the year. On a larger time scale, natural licks may lose their function when new sediments cover exposed materials that attract the animals. However, animals ar e not passive in relation to natural lick

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112 availability. If a lick is covered by somethi ng that animals can remove, they probably will do it over time. For example, we observed that a few months after the dense crown of a large fallen tree covered a natural lick, an imals reopened it by continuous use. In summary, natural licks in upland forest are a re liable source of minerals for the animals. Although sediments that form natural licks in the Yavari-Miri region have a large geographical extension, more recent sediment s cover them, and only the outcrop of those underlying, older sediments forms the actual li cks. The area available for animals to exploit is very small compared to the w hole extension of the habitat (Chapter 3). However, minerals obtained by animals are li kely critical for th eir nutrition. Poor nutrition reduces reproduction and survival, and overall limits population growth and persistence. This argument agrees with the pr ediction that area occupied by natural licks in the habitat is small relative to its effect on its users. In conclusion, natural licks in the Yavari Miri River region are resources used by a relative large proportion of the wildlife community, they provide mineral nutrients that are in short supply (at least to some sp ecies) and, even though they occupy a proportionately small area, they may be critic al for abundance and persistence of animals in the area. The keystone role of a resource is not a concept applied to humans. However, humans are an integral part of ecosystems, and their use of natural resources has a tremendous impact on those ecosystems (M cDonnell & Pickett 1993). Addressing the importance of natural licks as a resource for human communities using the conceptual framework above provides comm on criteria for the analysis and helps to discuss the conservation implications of this research.

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113 Adapting the conceptual framework used above, the following results would be expected if natural licks can be considered as a keystone resource for people in western Amazonia: (1) a high proportion of people use natural licks (as an adaptation of the criterion of degree of consumer specificity, but applied to only one species-humansand quantification of importance in terms of number of persons using the licks rather than number of species), (2) natural licks provide something to its users that is in short supply and is not easily substitutabl e (low redundancy), and applied to people, it refers to game species, (3) natural licks are a reliable res ource (provide game when used), and (4) area occupied by natural licks is small relative to the benefits they provi de to their users. Examination of such predictions comes from the information gathered at the Nueva Esperanza village, a rural co mmunity of the Yavari-Miri River (Chapter 5). We found that 70% of hunters of the village regularly us e natural licks as hunti ng sites. Also, more than 40 natural licks are used within hunti ng areas, and many are regularly visited, not only for direct hunting, but also for getting in formation on some species in the area. This result agrees with the prediction that a hi gh proportion of hunters use natural licks. Also, we found that natural licks were the most important hunting sites for harvesting lowland tapirs. This ungulate species is the largest terr estrial mammal in the Amazon ecosystem, and it is naturally at lowe r densities than othe r species. Hunting lowland tapirs on forest trails is more difficult, since direct sightings in the forest are very rare. In fact, the encounter rate of tapirs have been estimated at 1.17 individuals per 100 km (Salaovaara et al 2003) in an area with very low hunting pressure, and is much lower in heavily hunted sites. However, lowland tapi r visitation rate to natu ral licks is higher in proportion to its abundance in the area (Chapter 2) and this feature is used to benefit the

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114 hunters. This result agrees with the pred iction than natural licks provide hunters something that is of limited supply in the area, as applied to lowland tapirs as compared to other prey. Also, concentrati on of other animals in the licks is another direct benefit for hunters. In addition, many hunters see natural licks as a reliable site for hunting, because of the high probability of finding a prey. However, reliability of hunting at licks depends on several factors, including hunting pressure and location of the most us ed licks. Licks that are heavily hunted are usually abandoned by animals and become less reliable. Also, most licks used by hunters are those close to the river because of easy access. Many of those licks may become flooded during the high water season (Chapter 3) and, as discussed above, they will not be as reliabl e all year round. This is probably the reason why many hunters indicated that they use licks more during the low water season. These observations agree with the prediction that na tural licks are a reliab le resource, although in a seasonal manner because of river level fluctuations. Also, natural licks are proportionately sm all compared to the whole hunting area, and yet they provide a significant proportion of the game in terms of biomass. Hunters of Nueva Esperanza village obtained about 30% of the harvested biomass either from licks or nearby riverbanks in 2002 (Chapter 5). Th ese results agree with the prediction that area occupied by natural licks is small relative to the benefits they provide to the hunters. In conclusion, natural licks in the Yavari -Miri River are a resource used by a large proportion of hunters of Nueva Esperanza vill age, the largest of the 4 small human communities in the area. Also, natural licks facilitate the hunting of one the largest game species, whose low density makes it difficult to find it on hunting trai ls. Finally, although

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115 natural licks occupy only a small proportion of hunting areas, they provide significant benefits to hunters in terms of harvested biomass. Also, natural licks have an effect on wildlife nutrition and health, which may result in a high ca rrying capacity of the area, which in turn benefits the people who use wildlife as a source of subsistence. Overall, several findings of this study ag ree with some of the ecological attributes expected from a keystone resource, for bot h wildlife and people in western Amazonia. However, further research is needed to examine the role of natural licks for all their users, and to better understand lowl and tapir mineral nutrition. Important conservation implications can be derived from the results of this dissertation. The Yavari-Miri Ri ver region is currently the mo st important source area (in a source-sink model) for replenis hment of heavily hunted sites of this part of the Peruvian Amazon. For the Yavari-Miri region to eff ectively work as a source its wildlife populations should be near ca rrying capacity (Pulliman 1988) so animal dispersal can replenish hunted (or sink ) areas. This is particularly im portant for species that are very vulnerable to over-hunting, such as lowland tapirs. Currently, settlers of Nueva Esperanza vi llage are involved in a community-based management process. Appropriate management of the licks should be stressed in that process. We recommend regulation of hunting at licks by temporal rota tion of use, and to ensure that large areas are maintained w ith low hunting pressure. Those areas should serve as a source to hunted area s, and should be of the best quality to ensure high animal densities. The existence of natural licks should be taken in to account as a key attribute of habitat quality when selecting source areas for wildlife conservation in western Amazonia.

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116 LIST OF REFERENCES Abrahams, P. W. 1999. The chemistry and minera logy of three savanna lick soils. Journal of Chemical Ecology 25: 2215-2228. Acosta, H., J. Cavalier and S. Londoo. 1996. Apor tes al conocimiento de la biologa de la danta de montaa, Tapirus pinchaque en los Andes centrales de Colombia. Biotropica 28: 258-266. Alvard, M. S., J. G. Robinson, K. H. Redfor d and H. Kaplan. 1996. The sustainability of subsistence hunting in the Neotropi cs. Conservation Biology 11: 977-982. Ammerman, C. B., D. H. Baker and A. J. Lewis. 1995. Bioavailability of nutrients for animals: amino acids, minerals and vitamins. Academic Press. San Diego. Antunez, M. S. 2001. Informe Tcnico No. 2, Proyecto Co-manejo comunal de fauna silvestre en la Rerserva Comunal Tams hiyacu-Tahuayo y la zona del ro Mir. WCS, Loreto. Iquitos, Peru. Unpublished report. Atwood, T, and H. P. Weeks, Jr. 2002. Sex-a nd age-specific pattern s of mineral lick use by white-tailed deer ( Odocoileus virginianus ). American Midland. Naturalist148: 289-296. Ayres, J. M. and C. Ayres. 1979. Aspectos da caa no alto rio Ar ipuana. Acta Amazonica 9: 287-298. Barongi, R. 1992. Husbandry and conservati on of tapirs. International Zoo Yearbook 32:7-15. Begazo, A. 1999. Hunting of birds in the Peruvian Amazon. PhD. Dissertation. University of Florida, Gainesville. Bennett, E. L. and J. G. Robinson. 2000. Hun ting for sustainability: the start of a synthesis. Pages 499-519 in J. G. Robi nson and E. Bennett, editors. Hunting for Sustainability in Tropical Forests. Co lumbia University Press. New York. Bicca-Marques, J C. and C. Calegaro-Marques. 1994. A case of geophagy in the black howling monkey Alouatta caraya. Neotropical Primates 2: 7-9. Bissonette, J. A. and P. R. Krausman. 1995. Integrating people and wildlife for a sustainable future. The Wildlife Society. Bethesda.

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117 Bodmer, E. 1989. Frugivory in Amazon ungulates Ph.D. Dissertation, University of Cambridge, Cambridge. Bodmer, R. E. 1990. Fruit patch size a nd frugivory in the lowland tapir ( Tapirus terrestris ). Journal of Zoology 222: 121-128. Bodmer, R. E. 1991. Influence of diges tive morphology on resour ce partitioning in Amazonian ungulates. Oecologia 85: 361-365. Bodmer. R. E. 1994. Managing wildlife with local communities in the Peruvian Amazon: The case of the Reserva Comunal Tamshiyacu-Tahuayo. Pages 113-134 in D. Western and M. Wright, editors. Natural Connections. Perspectives in communitybased conservation. Island Press. Washington, D.C. Bodmer, R. E., R. Aquino, P. Puertas, C. Reyes, T. Fang and N. Gottdenker. 1997a. Manejo y uso sustentable de peccaries en la Amazonia peruana. Occasional paper of the IUCN Species Survival Commission No. 18. Bodmer, R. E., J. F. Eisenberg and K. H. Redford. 1997b. Hunting and the likelihood of extinction of Amazonian mammals. Conservation Biology 11: 460-466. Bodmer, R. E. and P. E. Puertas. 2000. Co mmunity-based co-management of wildlife in the Peruvian Amazon. Pages395-409 in J. G. Robinson and E. L. Bennett, E., editors. Hunting for Sustainabi lity in Tropical Forests. Columbia University Press, New York. Bodmer, R. E. and P. Puertas. 2003. A brief history of the Yavari Valley. Pages 172-176 in N. Pitman, C. Vriesendorp, D. Mo skovits, editors. Peru: Yavar. Rapid Biological Inventories Report 11. The Field Museum, Chicago. Bodmer, R. E., P. Puertas and M. Antnez. 2003. Use and sustainability of wildlife hunting in and around the proposed Yavari Reserved Zone. Pages 178-185 in N. Pitman, C. Vriesendorp, D. Moskovits, editors. Peru: Yavar. Rapid Biological Inventories Report 11. The Field Museum, Chicago. Bodmer, R. E, P. Puertas, L. Moya and T. Fang. 1993. Evaluacin de las poblaciones de tapir de la Amazonia Peruana: Fauna en camino de extincin. Boletin de Lima 88: 33-42. Brady, N. C. 1974. The nature and properties of soils. 8th edition. Macmillan Publishers, New York. Bray, R.H., and L.T. Kurtz. 1945. Determination of total, organic, and available forms of phosphorus in soils. Soil Science 59:39-45. Calef, G. W. and G. M. Lortie. 1975. A mineral lick of the Barren-ground caribou. Journal of Mammalogy 56: 240-242.

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118 Caughley, G. and A. R. E. Sinclair. 1994. W ildlife Ecology and Management. Blackwell Scientific Publications. Oxford. Clayton, L. and D. W. MacDonald. 1999. So cial organization of the babirusa ( Babyrousa babyrussa ) and their use of salt licks in Sulawesi, Indonesia. Journal of Mammalogy 80:1147-1157. Couturier, S. and C. Barrete. 1987. The behavi or of moose at natural mineral springs in Quebec. Canadian Journal of Zoology 66: 522-528. Del Campo, H., Z. Valverde, A. Calle a nd A. Wali. 2003. Human Communities. Pages 165-171 in N. Pitman, C. Vriesendorp, D. Moskovits, editors. Peru: Yavar. Rapid Biological Inventories Report 11. The Field Museum, Chicago. Diamond, J., K. D. Bishop and J. D. Gilard i. 1999. Geophagy in New Guinea birds. Ibis 141: 181-193. Downer, C. C. 2001. Observations on the di et and habitat of the mountain tapir ( Tapirus pinchaque ). Journal of Zoology 254: 279-291. Eisenberg, J. F. 1989. Mammals of the Neotropi cs: the northern Neotropics. University of Chicago Press, Chicago. Emmons, L. H. 1987. Comparative feeding ecology of felids in a Neotropical rain forest. Behavioural Ecology and Sociobiology 20: 271-283. Emmons, L. H. and F. Feer. 1997. Neotropi cal Rainforest Mammals. A field guide. Second edition. The University of Chicago Press, Chicago. Emmons, L. H. and N. M. Stark. 1979. Elemen tal composition of a natural mineral lick in Amazonia. Biotropica 11:311-313. Erard, C. and M. Sabatier. 1994. Fruit eating and ornithocory in the forest of Guyana: the example of large terrestrial birds and Marail guan. Alauda 62: 27-31. Ferrari, S. F. 1995. Observations on Chiropotes albinasus from the Rio dos Marmelos, Amazonas, Brazil. Primates 36: 289-293. Fleming, T. F.1988. The short-ta iled fruit-bat. University of Chicago Press, Chicago. Foerster, C. 1998. Ecologa de la danta centroamericana Tapirus bairdii en un bosque hmedo tropical de Costa Rica. Master Thesis, Universidad Nacional de Costa Rica, Heredia. Fragoso, J. M. V. 1997. Tapir-generated seed shadows: scale-depende nt patchiness in the Amazon rain forest. Journal of Ecology 85:519-529.

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119 Fragoso, J. M V. 1998. Home range and move ment patterns of white-lipped peccary ( Tayassu pecari ) herds in the northern Brazili an Amazon. Biotropica 30: 458-469 Fragoso, J.M. V. 1999. Perception of scale and resource partitioning by peccaries: behavioral causes and ecological imp lications. Journal of Mammalogy 80: 9931003. Fragoso, J. M. V. and J. M.Huffman. 2000. Seed-dispersal and seedling recruitment patterns by the last Neotropical megafaunal element in Amazonia, the tapir. Journal of Tropical Ecology 16: 369-385. Fragoso, J. M V, K. M. Silvius and J. A. Correa. 2003. Long-distance seed dispersal by tapirs increases seed surv ival and aggregates tropi cal trees. Ecology 84: 1998-2006. Fraser, D. and H. Hristienko. 1981. Activity of moose and white-tailed deer at mineral springs. Canadian Journal of Zoology 59: 1991-2000. Galetti, M., A. Keuroghlian, L. Hanada a nd M. I. Morato. 2001. Frugivory and seed dispersal by the lowland tapir ( Tapirus terrestris ) in southeast Brazil. Biotropica 33: 723-726. Gentry, A. H. 1996. A field guide to the families and genera of woody plants of north west South America: (Colombia, Ecua dor, Peru): with supplementary notes. University of Chicago Press, Chicago. Gilardi, J. D., S. S. Duffey, C. A. Munn a nd L. A. Tell. 1999. Biochemical functions of geophagy in parrots: detoxification of diet ary toxins and cyto protective effects. Journal of Chemical Ecology 25: 897-922. Gilardi, J. D. and C. A. Munn. 1998. Pattern s of activity, flocking, and habitat use in parrots of the Peruvian Amazon. The Condor 100: 641-653. Grace, N. D., J. R. Rounce, and J. Lee. 1996. Effect of soil ingestion on storage of Se, vitamin B12, Cu, Cd, Fe, Mn and Zn in th e liver of sheep. New Zealand Journal of Agricultural Research 39: 325-331. Hebert, D. and I. M. Cowan. 1971. Natural sa lt licks as part of the ecology of the mountain goat. Canadian Journal of Zoology 49:605-610. Henry, O., F. Feer, and D. Sabatier. 2000. Diet of the lowland tapir ( Tapirus terrestris L.) in French Guiana. Biotropica 32: 364-368. Henshaw, J. and J. Ayeni. 1971. Some aspects of big-game utilization of mineral licks in Yankari Game Reserve, Nigeria. East African Wildlife Journal 9: 73-82. Heymann, E. W. and G. Hartmann. 1991. Geophagy in moustached tamarins, Saguinus mystax (Platyrrhini: Callitrichid ae), at the Rio Blanco, Peruvian Amazon. Primates 32: 533-537.

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120 Holdo, R. J. P. Dudley, and L. R. McDowe ll. 2002. Geophagy in the African elephant in relation to availability of dietary sodium. Journal of Mammalogy 83: 652-664. Hoorn, C. 1991. Nota geolgica; la formacin Pevas (“Terciario Inferior Amaznico”): Depsitos fluvio-lacustres del Mioceno medi o a superior. Colombia Amaznica 5: 119-130. Hoorn, C. 1993. Geologa del nororiente de la Amazonia peruana: la Formacin Pebas. Pages 69-85 in Kalliola, R., M. Puha kka and W. Danjoy, editors. Amazonia Peruana. Vegetacin Hmeda Tropical en el Llano Subandino. Proyecto Amazonia Universidad de Turky and Oficina Naciona l de Evaluacin de Recursos Naturales Finnish, Jyvskyl,. IGAC. 1990. Mtodos Analticos del Laboratorio de Suelos. Instituto Geogrfico Agustn Codazzi, Subdireccin Agrol oga. Bogot, 502 Pages Izawa, K. 1993. Soil eating by Alouatta and Atel es. International Jour nal of Primatology 14: 229-242. Janis, C. 1976. The evolutionary strategy of the Equidae and the origins of rumen and cecal digestion. Evolution 30: 757-774. Janssen, D. L., B. a. Rideout, M. S. Edwa rds. 1999. Tapir medicine. Pages 562-568 in M. E. Fowler and E. Miller, editors. Zoo a nd Wild Animal Medicine: Current Therapy 4. Saudenders, Philadelphia. Janzen, D. H. 1982a. Wild plant acceptabilit y to a captive Costa Rican Baird’s tapir. Brenesia 19-20: 99-128. Janzen, D. H. 1982b. Seeds in tapir dung in Santa Rosa National Park, Costa Rica. Brenesia 19-20: 129-135. Jarrige, R. and W. Martin-Rosset. 1981. Le cheval: reproduction, se lection, alimentation, exploitation. 13th Journes du Grenier Theix. Inst itut National de la Recherche Agronomique, Paris. Jones. R. L. and H. C. Hanson. 1985. Mineral licks, geophagy, and biochemistry of North American ungulates. The Iowa St ate University Press. Ames. Julliot, C. and D. Sabatier. 1993. Diet of the red howler monkey ( Alouatta seniculus ) in French Guiana. International Journal of Primatology 14:527-550. Kalliola, R. M., Puhakka, W. Danjoy. 1993. Amazonia Peruana, Vegetacin Hmeda Tropical en el Llano Suba ndino. Proyecto Amazonia, Univ ersidad de Turku. Turku. Kauffman, S, G. Paredes, R. Marquina. 1998. Su elos de la zona de Iquitos. Pages139-229 in R. Kalliola and S. Flores-Paitn, editors. Geoecologa y desarrollo Amaznico. Estudio integrado en la zona de Iq uitos, Per. Turun Yliopisto, Turku.

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128 BIOGRAPHICAL SKETCH Olga Lucia Montenegro was born in Bogot , Colombia. She graduated from the Department of Biology at the Universidad Nacional de Colombia in 1990. For five years she worked for a non-governmental institution in research and conservation issues in the Colombian Amazon. In the fall of 1996 she bega n graduate studies in the Department of Wildlife Ecology and Conservation at the Univer sity of Florida. On December 1998 she earned a Master of Science. She continued her studies in tropical wildlife at the University pursuing a Ph.D. degree through th e same department. After graduation, she plans to dedicate her time to academic and research work in the tropics.


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NATURAL LICKS AS KEYSTONE RESOURCES FOR WILDLIFE AND PEOPLE IN
AMAZONIA














By

OLGA LUCIA MONTENEGRO


A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY

UNIVERSITY OF FLORIDA


2004



























Copyright 2004

by

Olga Lucia Montenegro


























This dissertation is dedicated to the memory of my father, Jose J. Montenegro, from
whom I inherited his curiosity for animals, his love for nature and his spirit of adventure;

to my mother Blanca Lilia who, together with my father, gave me all the values that
guide my life;

to my brothers Alvaro and Gabriel, and my sisters Marlene and Doris and their beautiful
families, whose love and support are with me always; and.

to Don, whose love, friendship and encouragement help me to pursue my dreams.















ACKNOWLEDGMENTS

I would like to start by thanking my supervisory committee chair and co-chair, Dr.

Richard Bodmer and Dr. George Tanner. Dr. Bodmer provided valuable academic advice

during the whole process of completing my studies, and critical support for my fieldwork

in the Peruvian Amazon. Dr. Tanner helped me with valuable comments on my work and

important suggestions for my analyses and writing. Also, the other members of my

academic committee, Dr. Melvin Sunquist, Dr. Lyn Branch and Dr. Lee McDowell

provided significant suggestions and support during several stages of this study, and

critical review of previous versions of this document. A former member of my

supervisory committee, Dr John Eisenberg (deceased) provided important suggestions

and encouragement in the early stage of this study. Although he is not with us anymore,

his deep knowledge and his teachings have been of great value on our understanding of

tropical mammal ecology.

Many other people contributed in different ways to this study. Donald Mee

patiently reviewed several versions of this document, and helped me to improve it

significantly. His critical comments, philosophical discussions, and constant support have

been very important for me all these years.

Pablo Puertas, Miguel Antunez, and Kati Salovaara provided support and

companionship during the fieldwork. Also crewmembers of the research vessel Nutria,

Julio Curinuqui, Gilberto Asipali, Fredy Curinuqui and Jorge Pacaya, and field assistants

Tedy Alvarado, Juan Huanaquiri, Jose Arirama, Pablo Asipali and Oliver Rodriguez









helped during our work in the Yavari-Miri River. During year 2002, Colombian master

student Carolina Lozano joined the expedition and helped in many ways with the

fieldwork. During the same year also, Jairo Huanaquiri of Village Esperanza, provided

very important help, going with us along the Esperanza Creek and Yavari-Miri River,

mapping and measuring natural licks. His sense of humor and knowledge of the area and

the animals made of the fieldtrip a fun and productive experience.

Community members of Villages Esperanza, San Felipe and Carolina, on the

Yavari-Miri River kindly received us in their homes and shared with us their experiences,

knowledge and friendship. They also shared with us their masato (a fermented drink),

soccer games, and parties, making us feel welcome and at home.

In Iquitos, Roberto Pezo, dean of Biological Sciences Department of Universidad

Nacional de la Amazonia Peruana, provided institutional support. Also, Nancy Arevalo,

former director of Herbarium Amazonence, kindly let us reviewing our plant material at

the herbarium, and botanist Juan Ruiz provided important help with plant identification.

In Colombia, Hugo L6pez, assistant professor at Universidad Nacional de

Colombia greatly contributed in several forms to this study, both in Leticia and Bogota,

with critical suggestions, and in kind support and friendship. Also, Gonzalo Andrade,

director of Instituto de Ciencias Naturales provided institutional support. Professor

German Palacio, director of Instituto Imani, at Universidad Nacional de Colombia at

Leticia, also helped with some of the logistics. Also at Leticia, Juan Echeverri, Martha

Pab6n, Pablo Palacios, Carlos Zarate and Edwin Agudelo gave support in the early stages

of the fieldwork. Fundaci6n Terrapreta, in Bogota, assisted with the soil analyses, and

soil scientist Pedro Botero, helped with the interpretation of results. Corporaci6n









Colombiana de Investigaci6n Agropcuaria CORPOICA, helped with plant and tapir

fecal mineral analyses.

Also, in Colombia many colleagues and friends helped me on different occasions.

Dr. Alberto Cadena, former curator of the mammal laboratory of the Museum of Natural

History at Universidad Nacional de Colombia was my first mammal professor and greatly

inspired my interest in this group of animals. He always encouraged us to keep studying

and increasing our understanding of our wild animals. Pedro Sanchez, assistant professor

of Biology gave me encouragement and valuable friendship. Marcela Gomez, Francisco

Sanchez, Alba Lucia Morales, and Manuel Paez helped me to prepare some of the

materials for the fieldwork. Juliana Rodriguez helped me on several occasions in

processing part of my samples. Aida Otalora, Silvia Alvarez, and Elizabeth Meza helped

in entering or reviewing some of my data files. Patricia Medici, chair of the Tapir

Specialist Group (TSG) of IUCN, Diego Lizcano and other members of TSG shared with

me their knowledge on tapirs and provided several opportunities to present and discuss

preliminary results of this study. My friend German de la Hoz taught me many things and

I will always be grateful for his support.

In Gainesville, many people helped me in several ways to successfully complete

this study and my academic work at the University of Florida. Dr. Nat Frazer, chair of the

Department of Wildlife Ecology and Conservation provided essential support at the

department. Faculty and staff were also very helpful in all stages of this process and

always provided me rapid and efficient solution to any difficulty, when needed. My

friends at University of Florida, Maria Ines Barreto, Carlos Jaramillo and Cristina Dockx

helped me with handling part of my field equipment and ensured that it reached me in the









field. Also, other friends at UF, Marcela Machicote, Sonia Canavelli, Ivan Diaz, Santiago

Espinosa, Alejandro Paredes, Luis Ramos and Margo Stoddard listened to my

monologues about my research and provide me with great suggestions. Matthew Bokach

patiently oriented me with ArcView. My officemates and friends Christine Lucas, Ian

Fiske, Matthew Trager, Chantavy Vongkhamheng, and Maynard Hiss also provided good

insights and great companion. Martha Castafieda, Victoria Mejia, Diana (Tita) Alvira,

Mutsuo Nakamura and other friends also made of my live in Gainesville a very enjoyable

experience. James Albury from the Center for Instructional and Research Computing

Activities (CIRCA) at University of Florida helped me in the final formatting and

electronic submission of this dissertation.

Several institutions provided funding for this study. The Tropical Conservation and

Development Program of the Center for Latin American Studies at University of Florida

provided a preliminary fieldwork travel grant. Idea Wild supported my work by donating

3 camera traps. The Columbus Zoological Park Association provided two research

awards in 2001 and 2002 for partial funding of some components of this study, including

equipment and expenses related to laboratory analyses. Wildlife Conservation Society

provided financial support to the research and conservation program coordinated by Dr.

Richard Bodmer, within which this study was conducted. Collection and research permits

were issued by the Institute of Natural Resources, INRENA, in Peru.

My studies at the University of Florida were supported by several sources.

Fulbright Commission and LASPAU provided me a fellowship for my master program.

The Tropical Conservation and Development Program of the Center for Latin American

Studies, the Department of Wildlife Ecology and Conservation and the Florida Museum









of Natural History provided me on different occasions with research, extension and

teaching assistantships that allowed me to pursue a Ph. D. degree. In Colombia,

COLFUTURO provided important financial support during the last year of my studies at

University of Florida. Finally, my family has always supported me in all my decisions

and has given me its love and support. This research and my studies at the University of

Florida would not have been possible without the support from all the above people and

institutions, and I am deeply grateful to all of them.
















TABLE OF CONTENTS



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

LIST OF TABLES ................................................... xii

LIST OF FIGURES ................................................ xiv

A B S T R A C T ..................................................................................................................... x v i

CHAPTER

1 IN T R O D U C T IO N .................................................. .. ....................................1.. .. ... 1

2 NATURAL LICK USE BY AMAZONIAN WILDLIFE IN NORTHERN PERU ..... 7

In tro d u c tio n ................................................................................................................... 7
S tu d y A re a .......................................................... ................................................ 9
M e th o d s ..................................................................................................... .............. 1 1
C am era T rapping .... .. ......................................... ........................ . ........... 12
Direct Observation ................................................................................... 12
E xam ining T racks... .. .......................................... ....................... ... .......... 13
D ata A n aly ses ...................................................................................................... 13
L ick visitors ......................................................................................... 13
Frequency of natural-lick use .................................................. ................ 13
Lick-visitation rate and species abundance............................................ 15
R e su lts....................................................................................................... ....... .. 15
L ic k V isito rs ........................................................................................................ 1 5
Frequency of Natural-Lick Use ..................................................................... 16
C am era traps ................................................................... . ........... 16
D irect observation ... .. .......... ......... ............................................. 17
E xam ining tracks ............................................... ............ .... .. .. ............ 18
Variation in Lick Use through the Year ......................................................... 18
Lick-Visitation Rates and Species Abundance.............................................. 18
D isc u ssio n ............................................................................................................... ... 1 9
L ic k V isito rs ........................................................................................................ 19
F frequency of L ick U se ..................... ............................................................. 23
Lick-Visitation Rate and Species Abundance ................................................25
Sum m ary and C conclusions ......................................... ........................ ................ 25









3 NATURAL LICK SOILS AS SOURCE OF MINERALS FOR WILDLIFE IN THE
Y A V A R I-M IR I R E G IO N ..........................................................................................34

In tro d u ctio n ................................................................................................................. 3 4
S tu d y S ite ................................................................................................................. ... 3 7
M e th o d s ................ .... ......................................................................................... 3 9
L ick L location and D description ................................................... .... ................ 39
Physical and Chemical Characterization of Lick Soils .................................39
Soil sam pling ................................................................... .... ......... 39
Laboratory analyses..................................... .. .......... .......... ................. 40
D ata analy sis ........................................................................................ 4 1
R e su lts................... .............. ................................................................... ....... .. 4 1
L ick L location and D description ....................................................... ................ 41
Physical and Chemical Characterization of Lick-Soils..................................43
Particle size ........................ .. ........................... 43
Chemical properties of lick and non- lick soils.......................................43
D isc u ssio n ................. ... ... ...................................................................................... .. 4 5
Lick Location and Description .............. ..... ... ................45
Physical and Chemical Characterization of Licks..........................................47
Particle size ........................ .. ........................... 47
Chemical properties of lick and non- lick soils.......................................48
Sum m ary and C conclusions ......................................... ........................ ................ 52

4 BROWSE AND FRUIT AS A SOURCE OF MINERALS FOR LOWLAND
TAPIR IN THE YAVARI-MIRI REGION...........................................................58

In tro d u ctio n ............................................................................................................... .. 5 8
S tu d y A re a ................................................................................................................. 6 2
M eth o d s ...................... ... ... .. ......................................................... ............. 62
Lowland Tapir Diet in the Yavari-Miri Region .............................................62
Determination of Minerals in Tapir Food and Fecal Samples .........................64
D ata A n aly ses ...................................................................................................... 6 5
R e su lts ...... ................. ... ..... .................................... ............................... 6 6
Lowland Tapir Diet at the Yavari-Miri Region..............................................66
M inerals in Low land Tapir Food .................................................... ................ 67
D iscu ssion .......................................................................... .................... .... ........... 7 0
Lowland Tapir Diet at the Yavari-Miri Region..............................................70
M inerals in Low land Tapir Food .................................................... ................ 72
Sum m ary and C conclusions ......................................... ........................ ................ 76

5 NATURAL LICKS AND RURAL PEOPLE OF THE AMAZON ...........................86

In tro d u ctio n ................................................................................................................. 8 6
S tu d y A re a .............. .. .. .. ...................................................................................... .. 8 8
L location and B iophysical Setting................................................... ................ 88
History and Description of Nueva Esperanza Village ................ ..................... 88
M e th o d s ................................................................................................................. . 9 1


x









Subsistence H hunting R records ......................................................... ................ 91
Natural Lick M apping and Description ................ ................................... 92
Hunters' Perceptions Concerning Natural Licks............................................92
R results ...................... .. .... .. ...................................... 93
Subsistence Hunting in Nueva Esperanza Village ........................................93
Natural Lick M apping and Description ................ ................................... 94
Hunters' Perceptions Concerning Natural Licks............................................95
D isc u ssio n ................. ... .................................................................................... ... 9 6
Subsistence H hunting R records ......................................................... ................ 96
Natural Lick M apping and Description ................ ................................... 98
Hunters' Perceptions Concerning Natural Licks............................................99
Sum m ary and C conclusions ................. .......................................................... 101

6 SYNTHESIS AND CONCLUSIONS .......... ..........................110

LIST O F R EFEREN CE S ... ................................................................... ............... 116

BIOGRAPH ICAL SKETCH .................. .............................................................. 128















LIST OF TABLES


Table page

2-1 Sampling effort used in three detection methods to determine the frequency of
natural-lick use by wildlife in the Yavari-Miri River Valley, during year 2001......26

2-2 Sampling effort used in direct observation per season........................ ............... 26

2-3 Species detected at natural licks by camera trapping, direct observations and
tracks in the Yavari-Miri River valley, Peruvian Amazon..................................27

2-4 Number of monthly photo-captures at 14 licks form March to December 2001,
in the Yavari-M iri River Valley, Peruvian Amazon ........................... ................ 28

2-5 Frequency of birds and mammals observed at eight natural licks from February
to early December (excluding August), 2001 in the Yavari-Mirin River Valley,
Peruvian Amazon. ....................... .. .......... ............ ............... 29

2-6 Chi-square values for testing the null hypothesis that number of sightings is the
sam e in the three seasons ......................................... ........................ ................ 30

3-1 Number of soil samples from lick and non-lick sites gathered in year 2001 in the
Yavari-M iri River valley in the Peruvian Amazon. ............................ ................ 53

3-2 Descriptive features of 24 natural licks in the upper Yavari-Miri River valley,
Peruvian Amazon. ... ................................ ........ .... ............... 54

3-3 Chemical characterization of soils from lick and non-lick sites in two seasons of
year 2001 in the Yavari-Miri River valley in the Peruvian Amazon. ....................55

3-4 Microminerals in lick and non-lick soils during the high water season of 2001,
in the Yavari-Miri River valley in the Peruvian Amazon ..................................56

4-1 Plant species in tapir browse along the Yavari-Miri River, Peruvian Amazon. ......78

4-2 Number of composite samples of each family analyzed for mineral
concentrations in 2 seasons in the Yavari-Miri River valley, Peruvian Amazon. ...80

4-3 Fruits in lowland tapir diet in the Yavari-Miri River valley, northeastern
Peruvian Amazon. ......... ................ .. ......... ............ ..........81..........8 1









4. 4 Mean content of nitrogen and macrominerals in tapir foods (browse and fruits),
suggested requirements (based on guidelines for horses) and mean
concentrations of excreted N and macrominerals in tapir feces...............................82

4-5 Mean content of microminerals in tapir foods (browse and fruits), suggested
requirement (based on guidelines for horses) and mean concentrations of
excreted m icrom inerals in tapir feces.................................................. ................ 83

5-1 Species hunted by settlers of Nueva Esperanza Village in the Yavari-Miri River
from January to December 2001. ...... ......... ......... ...................... 103















LIST OF FIGURES


Figure page

2-1 Location of 24 natural licks found in the Yavari-Miri RiverValley,
northeastern Peru ..................... ............ ............................. 30

2-2 Photo-captures per 100 trap-night per species at 14 licks from March to
December 2001 in the Yavari-Mirin River Valley, Peruvian Amazon (excludes
b ats). ....................................................................................................... .......... 3 1

2-3 Total sighting rate of bird species at 8 licks surveyed from February to early
December 2001 in the Yavari-Miri River Valley, Peru. ............... ..................... 31

2-4 Total sighting rate of diurnal mammal species at 8 licks surveyed from February
to early December 2001 in the Yavari-Miri Valley, Peru............... ................32

2-5 Total sighting rate of nocturnal mammal species at 8 licks surveyed from
February to early December 2001 in the Yavari-Miri Valley, Peru......................32

2-6 Ratio of track occurrences for tapir (Tapirus terrestris), white-lipped peccary
(Tayassupecari), collared peccary (Pecari tajacu), and red-brocket deer
(M azam a am ericana) .. ..................................................................... ................ 33

2-7 Density of selected mammals in the Yavari-Miri River valley and their overall
lick-visitation rate during year 2001 ................................................... ................ 33

3-1 Location of the study site in the Yavari-Miri River valley, in northern Peruvian
A m a z o n ............................................................................................................... .. 5 6

3-2. Mean content of sand, silt and clay in samples from lick and non-lick soils. Size
of vertical lines indicates + 1 standard deviation. ............................... ................ 57

4-1 Percent distribution of plant families browsed by lowland tapir
(Tapirus terrestris) in the Yavari-Miri River valley, of the northeastern
Peruvian Amazon .................................. ............................. 84

4-2 Percentage of occurrence of several fruit species in lowland tapir feces along the
Yavari-M iri River valley, Peruvian Amazon. ..................................... ................ 84

4-3 Concentration of macrominerals in tapir browse, during high water and low water
seasons in the Yavari-Miri Rivier valley, Peruvian Amazon...............................85









4-4 Concentration of trace minerals in tapir browse during high water and low water
seasons in the Yavari-Miri River valley, Peruvian Amazon...............................85

5-1 Location of the study area in the Yavari-Miri River region, northeastern
Peruvian Amazon. ... ..................... ........ ...................105

5-2 Gender and age composition of Nueva Esperanza Village in the Yavari-Miri
River region, northeastern Peruvian Amazon (census conducted in 2002). .........106

5-3 Percent contribution of each species to the total number of animals hunted in
2001 in the Y avari-M iri River ...... ............. ............ ..................... 106

5-4 Percent contribution of each species to the total biomass hunted in 2001 in the
Y avari-M iri R iver ... ..................................................................... .............. 107

5-5 Proportion of biomass harvested by hunters of the Nueva Esperanza Village per
hunting site from January to December 2001. ...................................... 108

5-6 Biomass hunted per ungulate species at riverbanks, natural licks and hunting
trails in the Yavari-Miri River region during year 2001 ................................108

5-7 Location of hunting areas and natural licks used by settlers of Nueva Esperanza
v illa g e ................................................................................................................ .... 1 0 9















Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy

NATURAL LICKS AS KEYSTONE RESOURCES FOR WILDLIFE AND PEOPLE IN
AMAZONIA

By

Olga Lucia Montenegro

December 2004

Chair: Richard E. Bodmer
Cochair: George Tanner
Major Department: Wildlife Ecology and Conservation

Natural licks are particular sites in some types of habitats often visited by a number

of wild animals with the purpose of licking or consuming soil (a behavior known as

geophagy). Several studies associate geophagy with the nutritional ecology and/or health

of the animals that use them. Therefore, the existence of natural licks in a particular

habitat may reduce the costs of obtaining adequate nutrition, and/or maintaining health;

and thus may be fundamental to population persistence. One of the habitats where natural

licks exist is the Amazon forest. Many Amazonian wildlife species, including large birds

and herbivorous mammals, are users of natural licks. Natural licks also may be important

for rural communities that rely on wildlife for their subsistence. This is particularly

important for Amazonian human communities, because one of the most common hunting

techniques in those forests is waiting for game animals at natural licks.









Our study addressed the importance of natural licks for both wildlife and humans in

the Yavari-Miri River valley in the northeastern Peruvian Amazon. A relatively large

group of mammalian and large bird species frequently visited natural licks during 2001.

The most frequent lick visitors were lowland tapirs. Natural licks found in the Yavari-

Miri River valley had higher concentration of several minerals (Na, Ca, Mg, P, Cu, S, and

B) compared to non-lick samples. Those differences were constant throughout the year;

suggesting that natural licks are in fact, a source of minerals for wildlife in the Yavari-

Miri River valley. The diet of the most-frequent lick visitor (the lowland tapir) was

examined for mineral content. Results showed that combined foods eaten by lowland

tapirs are of good quality regarding mineral content, except for Na, P, Cu and Zn. We

suggest that tapirs supplement their mineral intake by consuming mineral-rich soils at

natural licks in the Yavari-Miri River valley. The above results suggest that natural licks

are a key resources for several Amazonian species because they represent a natural

mineral source in the humid forest of western Amazonia.

To assess the importance of natural licks for Amazonian human communities,

subsistence-hunting patterns were examined at the Nueva Esperanza village, in the

Yavari-Miri River valley. Over 30% of total biomass hunted during 2001 was harvested

at licks, and was heavily represented by lowland tapirs. Hunters of Nueva Esperanza

village use more than 40 natural licks located along the Esperanza Creek and the middle

and lower Yavari-Miri River. We recommend regulation of hunting at licks by temporal

rotation of use. Also, we suggest that natural licks should be an attribute of habitat quality

when selecting areas for wildlife conservation in western Amazonia.














CHAPTER 1
INTRODUCTION

In wildlife ecology, a resource has been simply described as "something an animal

needs" (Caughley & Sinclair 1994:46). The conservation biology discipline has

introduced the term keystone resources to refer to those resources that are critical or

limiting in particular habitats, but are crucial for many species in a community (Primack

1993). The above concept is an extension of the keystone term used in other contexts.

The term keystone was first used in ecology to refer to a predator species of exceptional

importance because of its critical effect on prey populations in maintaining the structure

of its community (Paine 1969). Since then, the concept of a keystone species has been

extended to many species across trophic levels, and has been categorized according to

their function and community importance (keystone predator, prey, mutualist, host,

modifier; Mills et al. 1993). Power et al. (1996:609) proposed a refined definition for the

keystone as "a species whose impact on its community or ecosystem is large, and

disproportionately large relative to its abundance". The keystone role has been extended

not only to species (both plants and animals), but also to critical limiting resources that

"occupy only a small area of the habitat, and yet are critical to many species in the

community" (Primack 1993:48).

Natural licks are listed among those keystone resources (Primack 1993). Natural

licks are particular sites in some types of habitats often visited by a number of wild

animals with the purpose of licking or consuming soil. This behavior, known as

geophagy, is common among many mammals ungulatess, primates, rodents) and several









species of birds. Geophagy has been reported in many geographical locations throughout

the world.

Because ingested soils usually have a high content of one or several minerals

and/or a higher clay content compared to non-eaten soils, several benefits of geophagy

have been proposed. One hypothesis is that minerals in lick soil compensate for mineral

deficiencies or imbalances (Jones & Hanson 1985). This is why researchers usually refer

to geophagy sites as mineral licks or salt licks. Another hypothesis is that the clay in

eaten soil has beneficial effects on decreasing acidosis, secondary plant compounds,

intestinal infections or parasites (Mahaney 1993; Mahaney et al. 1996, 1997; Gilardi et

al. 1999). Those studies refer to the licks as clay licks.

These hypotheses may not be mutually exclusive. Comparing data across studies is

difficult because of the different research questions and methods used in each case

(reviews in Kreulen 1985; Klaus & Schmid 1998; Diamond et al. 1999; Krishnamani &

Mahaney 2000). The overall conclusion of those reviews is that geophagy has different

functions for different animal species, and/or different functions for the same species

under different situations. However, all proposed reasons for soil consumption at natural

licks (as are called hereafter) seem related to the nutritional ecology and/or health of the

animals that use them. Therefore, the existence of natural licks in a particular habitat may

reduce the costs of obtaining adequate nutrition, and/or maintaining health; and thus may

be fundamental to population persistence.

One of the habitats where natural licks exist is the Amazon forest, particularly in

western Amazonia. Many wildlife species (mainly ungulates, primates, and rodents, and

some birds species) are users of natural licks. Preliminary research in the Peruvian









Amazon indicated that during the dry season in the southern Peruvian Amazon, lowland

tapirs and other ungulates are frequent lick users (Montenegro 1998). However, it is

poorly known whether the use of licks is constant through the year, or occurs mainly

during dryer seasons. Also, in that pilot study, further research on dietary mineral

contents of lowland tapir food was suggested to better examine the mineral-intake

hypothesis for tapirs in the Amazon forest.

Natural licks also may be important for rural communities that rely on wildlife for

their subsistence. For many Amazonian rural communities, wildlife hunting continues to

be one of the most important subsistence sources (Robinson & Bodmer 1999). A

potential keystone role of natural licks for local hunters could be hypothesized, since one

of the most common hunting techniques in the Amazon forest is waiting for game

animals at natural licks. At the Tamshiyacu-Tahuayo Communal Reserve (RCTT) in the

Peruvian Amazon, the presence of natural licks, known as colpas, is often an

indispensable condition for establishing hunting sites (Puertas 1999). One important

hunting strategy used by local hunters at the RCTT is going to the colpas at night looking

for tapirs, deer and pacas (Puertas 1999). Moreover, Puertas (1999) provided one

example of a hunter strategically placing food in colpas to accustom animals to supplied

fruits. This practice allowed the hunter to rotate hunting sites over time.

Although the use of natural licks as hunting sites is commonly reported, few studies

have quantified the relative importance of those places in terms of the amount of game

obtained in relation to total hunting. The few published studies on this subject involve use

of licks by native groups. In the Colombian Amazon, for example, indigenous

communities of the Miriti-Parana River obtain about 25% of consumed meat from natural









licks (Walshburger & Hildebrand 1988). No other estimations of hunting return from

natural licks are published, and the real importance of licks as hunting sites is generally

poorly known in Amazonian hunting systems.

Over-hunting at natural licks was apparently controlled by social and ritual

practices in many indigenous communities. For many Amazonian communities, however,

such restrictions are no longer practiced, or are not part of their culture, especially for

settlers who migrated from other regions. As a result, hunting at natural licks is usually

uncontrolled. Often hunters report that a natural lick has been damaged when animals, as

a consequence of excessive hunting, no longer visit it.

Intensive hunting at natural licks drives animals away, probably affecting their

nutrition and health. Over-exploitation of many wildlife species also is contributing to

declines in their populations. This is particularly true for ungulates such as lowland tapirs

and large primates (Bodmer et al. 1993, 1997b). At the same time, over-exploitation of

wildlife at natural licks may threaten subsistence of rural communities that depend on

wildlife as their main source of subsistence. For the above reasons, a better understanding

of the importance of natural licks as a resource for Amazonian wildlife, and for rural

communities in the Amazon is needed in order to design effective wildlife-management

programs that take into account both rural communities' subsistence and long-term

wildlife persistence.

From the above background, these questions arise: how important are natural licks

for both wildlife and people in western Amazonia? Can they be considered as a keystone

resource in that habitat? Peres (2000) proposed that 4 ecological attributes could be

examined in order to help identifying putative keystone resources: (1) degree of









consumer specificity, (2) temporal redundancy, (3) reliability, and (4) abundance. From

the consumer's perspective, a keystone resource is one with low redundancy (available

when alternative sources are not), is consumed by a large proportion of the species

assemblage, is highly reliable, and has low abundance.

Although Peres (2000) proposed these attributes to identify putative keystone plant

resources, they appear useful to examine the potential keystone role of other resources.

For this reason, the above attributes are used here as a framework to examine the

importance of natural licks in western Amazonia. If natural licks can be considered a

keystone resource for both wildlife and people in western Amazonia, the following

results would be expected: (1) a high number of lick users (both wildlife and people) visit

the licks, (2) natural licks provide something to their users that is in short supply and is

not easily substitutable (low redundancy), (3) natural licks are a reliable resource (are

available when users need them), and (4) area occupied by natural licks in the habitat is

small relative to its effect on its users.

Our study addressed the importance of natural licks for both wildlife and humans in

a site of western Amazonia, the Yavari-Miri River valley of northeastern Peru. The study

is presented in 4 components addressing the following objectives:

* Objective 1: To identify the wildlife species that are the most frequent licks users,
to describe their pattern of visitation through the year, and to examine whether they
visit licks in proportion to their abundance in the Yavari-Miri River valley in
northeastern Peruvian Amazon.

* Objective 2: To evaluate natural licks as a source of minerals for Amazonian
herbivores, and to describe the licks in terms of their size and location in the
Yavari-Miri River valley.

* Objective 3: To examine the mineral intake hypothesis for lowland tapirs by
determining the mineral content of tapir food and tapir feces.









* Objective 4: To examine the importance of natural licks for subsistence hunting in
an Amazonian rural community, and its implications for management and
conservation.

The following hypotheses were tested:

* Hypothesis 1: A relatively large number of species use licks, at least during part of
the year.

* Hypothesis 2: For at least for some species, their use of natural licks is higher than
expected from their abundance in the area.

* Hypothesis 3: Soils at natural licks have higher mineral concentrations (at least for
one or more minerals) than non-lick soils.

* Hypothesis 4: Lowland tapir food is limited in one or more mineral nutrients in the
Yavari-Miri River valley and such limitation is constant through the year.

* Hypothesis 5: Excretion of limited minerals (at least for some minerals) is low in
tapir feces.

* Hypothesis 6: Hunting at natural licks provides a higher contribution to the overall
harvest, at least for some species, as compared to other hunting sites.

* Hypothesis 7: Most rural hunters in a community of western Amazonia use natural
licks as hunting sites

Chapter 2 addresses hypotheses 1 and 2, examining the pattern of natural lick use

by Amazonian wildlife in the Yavari-Miri River region. Chapter 3 deals with the

properties of consumed soils at natural licks, to examine hypothesis 3. Chapter 4

discusses browse and fruit as sources of minerals for lowland tapir, and mineral fecal

excretion, to address hypotheses 4 and 5. Chapter 5 describes the use on natural licks by a

rural community in the Yavari-Miri River, addressing hypotheses 6 and 7. Finally,

Chapter 6 presents a synthesis of results and its implications for wildlife conservation in

the Yavari-Miri River valley.














CHAPTER 2
NATURAL LICK USE BY AMAZONIAN WILDLIFE IN NORTHERN PERU

Introduction

Wildlife species around the world use natural licks. Many of those species are

either mammals (Klaus & Schmid 1998; Krishanmani & Mahaney 2000) or birds

(Diamond et al. 1999; Gilardi et al. 1999). Among mammals, ungulates visit natural licks

in diverse habitat types. Muskox and caribou in tundra (Calef & Lortie 1975; Klein &

Thing 1989), moose in boreal forests (Fraser & Hristieko 1981;Tankersley & Gasaway

1983; Couturier & Barrete 1987; Miller & Livitatis 1992), and white-tailed deer in many

locations in North America (Weeks & Kirkpatrick 1976, Atwood & Weeks 2002) are

some examples of ungulates using licks in temperate regions. For tropical areas,

information on lick use exists mainly for areas of the Old World. African elephants

(Holdo et al. 2002) and seven other ungulate species in savannas and woodlands

(Henshaw & Ayeni 1971), Asian elephant and other ungulates in tropical forest of

Thailand, and babirusa in Indonesia (Clayton & MacDonald 1999) are some large

mammals using natural licks in the tropics. Besides ungulates, more than ten species of

Old World primates are reported to eat soil from licks or the forest floor (Krishmamani &

Mahaney 2000).

Much less is known about natural lick use in the Neotropics. Few publications

exist, other than occasional reports of primates using licks (Heymann & Hartmann 1991;

Izawa 1993; Ferrari 1995; Miuller et al. 1997), tapir observations at a few sites (Pefia et









al. 1996, Montenegro 1998, Lizcano & Cavelier 2000), and a study on the physiological

significance of geophagy for some species of birds (Gilardi et al. 1999).

In both temperate and tropical regions, research dealing with natural lick use has

addressed soil consumption (or geophagy), and its physiological significance to the

animals. Several non-exclusive hypotheses transcend geographic areas and/or species

(Kreulen 1985; Klaus & Schmid 1998; Diamond et al. 1999; Krishnamani & Mahaney

2000). The overall view is that soil consumption at natural licks is linked to the

nutritional ecology (Chapter 4) and/or health of the lick users. Besides the benefits for the

animals' nutrition and/or health, licks may also function as animal-gathering places,

facilitating social encounters (Couturier & Barrete 1987, Ruggiero & Fay 1994).

Since natural licks may have more than one function for wildlife species, and those

functions may vary across species, licks may represent a resource whose ecological

importance goes beyond the particular benefits for individual species. As suggested by

Klaus & Schmid (1998), presence of natural licks in some habitats may have an effect on

population densities and structure, and may influence the carrying capacity of areas with

lick sites. Studies rarely discuss natural lick use at a community-wide level with a

broader ecological perspective. The ecological importance of natural licks could thus be

overlooked.

We need to know which species in a given region use licks, how often they use

them, and whether that use differs among species to assess the significance of licks as a

resource for wildlife in that region. In the Amazon rainforest, this knowledge is limited,

but it may have ecological and conservation implications.









This chapter examines the use of natural licks by wildlife species in the Yavari-

Miri River valley in the northeastern Peruvian Amazon. The following questions were

addressed:

* Question 1.Which species use natural licks in the Yavari-Miri River valley?

* Question 2.Do all species use licks with the same frequency, and does that
frequency vary through the year?

* Question 3. Do the species use licks in proportion to their abundance in the area?

These questions were addressed by inventorying all lick visitors, by comparing lick

visitation rates among species throughout the year, and by relating lick-visitation rates to

available data on species abundance. If natural licks are a resource of community-wide

importance in the Amazon forest, it is expected that a variety of species use licks, at least

during part of the year, and that at least for some species, their use of the licks is higher

than expected from their abundance in the area.

Study Area

The study area was located along the Yavari-Miri River, a tributary of the Yavari

River (Yavari District), Mariscal Ram6n Castilla Province, Department of Loreto, in

northeastern Peru. Fieldwork was conducted throughout the middle course of the Yavari-

Miri River, in the area between 430.23'S, 7226.69W and 4o24.77'S, 7209.76'W

(Figure 2-1). Weather stations on this river do not exist, but the area's climate conditions

were approximated from the closest stations in and around Iquitos (Marengo 1998), about

170 km northwest of the middle course of the Yavari-Miri River. The region is warm and

humid. Mean annual temperature is 26C, with monthly mean maximum temperatures

ranging from 28 to 30C, and monthly mean minimum temperatures from 17 to 20C.

Temperature drops below the minimum average for 3 to 5 days duringfriagem, an event









occurring between May and September, in which cold dry air masses coming from the

South Pole arrive in the Amazon basin (Marengo 1984). Mean annual precipitation

ranges from 2400 to 3100 mm (Marengo 1998), with the highest monthly rainfall

occurring from February to April (as high as 350 mm), and the lowest from June to

September (as low as 180 mm). Despite these monthly differences, there is no real dry

season (unlike more southern regions of the Peruvian Amazon). Monthly rainfall

differences are reflected in the Yavari-Miri and Yavari River water levels and discharge.

Water levels are lowest during the months of less rainfall (June to September), when sand

beaches appear along the riverbanks. The Yavari-Miri is a relatively narrow black-water

river, and could appear very shallow during the least-rainy months.

The Yavari region harbors remarkable plant diversity. Although vegetation in the

study site is still poorly known, about 1,600 plant species were identified during a recent

rapid biological inventory in the Yavari basin. Estimated total plant diversity in the

region is as high as 2,500 to 3,500 species (Pitman et al. 2003). This high diversity has

led the whole area to be considered as one of the centers of plant diversity (CPD) in

South America (Smithsonian Institute 2003). The three main geomorphic units in the

study area are terraces, alluvial plains, and sedimentary surfaces (Figure 2-1). Main

habitat types in the area are upland forests and flooded forests. Upland forests cover most

of the area, and exist on terraces and sedimentary surfaces. They are not uniform through

the area, with changes in plant composition occurring because of soil heterogeneity,

somewhat similar to the upland forest around Iquitos (Ruokolainen & Tuomisto 1998;

Pitman et al. 2003). Flooded forests exist on the alluvial plains of the Yavari-Miri and

Yavari rivers. Swamp forests (a type of flooded forest) are common along these rivers,









covering 25-50% of the flood plains (Pitman et al. 2003), and occur also on poorly

drained upland soils.

Animal diversity in the area is also high, especially for mammals, causing some to

consider the Yavari valley as one of the mammalian diversity hotspots of Peru (Valqui

1999, 2001; Salovaara et al. 2003). Although there is some hunting in the area, it is slight

compared to other sites in the Peruvian Amazon (Bodmer & Puertas 1999; Bodmer et al.

2003), and many wildlife species are still abundant. Lowland tapirs and other ungulates,

for instance, have healthy populations at the Yavari-Miri River (Salovaara et al. 2003).

Methods

An intense search for natural licks was conducted in the Yavari-Miri River valley

from January to March 2001. This search occurred along 66 km of trails opened on both

sides of the river. Trails were cut using predetermined bearings, based on characteristics

of the terrain observed from a satellite image. Areas around the trails were checked

carefully, especially when numerous tapir tracks were found, since they often indicate the

proximity of natural licks. Once a natural lick was found, its geographical coordinates

were taken with a global positioning system (GPS), and marked on a 1:100,000-scale

map.

This search yielded 21 licks, most of them found on the north side of the Yavari-

Miri River. Another 3 licks were found in July during a parallel study at the Yavari-Miri

River (Salovaara, in prep.), and were included in our study. All 24 licks were located on

the map (Figure 2-1). We monitored 7 to 24 licks from February to early December 2001

(except August), using 3 methods: camera trapping, direct observation, and examining

tracks.









Camera Trapping

Automatic 35-mm cameras triggered by a passive infrared motion detector were set

at selected licks. From March to July, three Buckshot passive infrared system cameras

(Buckshot35, Louisiana, USA) were used. From September to early December, two

additional CamTrakker (CamTrak South, Inc, Georgia, USA) cameras were available,

for a total of 5 cameras used in our study. Cameras were located at the entrance trails

and/or in front of the most-used sites of the licks, to increase the chance of every lick

visitor to be detected and photographed. Locations of the cameras were changed on

average of every 2 weeks to allow sampling of several licks. A total of 14 licks was

surveyed with 5 cameras (Table 2-1).

Direct Observation

At 7 licks, observation platforms (and sometimes blinds) were built to allow

observation without being seen by the animals. The area of platforms was 2.2 x 2.2 m,

and they were built 3 to 7 meters above the most-used sites of the licks. Palm leaves

were put around the platforms, to make them less visible. Those licks were monitored

from February or March through early December 2001 (except August). An additional

lick was added for direct observations from September, but no platform was built there.

Instead, observations were made from a hammock tied 10 m above the lick. With the

latter, a total of 8 licks was sampled by direct observation.

On average, 3 licks were observed per month (range, 1 to 7). Diurnal and nocturnal

observations were made at the licks. Total hours of observation were 796, of which 544

(68.3%) were nocturnal and 252 (31.7%) were diurnal. Total average observation time

per lick was 68 h at night (range, 12 to 144 h), and 31.5 h during the day (range, 7 to 69

h) (Table 2-1). Diurnal observations were made with binoculars. Nocturnal observations









were made with an ITT night vision scope. In some cases, a video camera was used to

record animals visiting the licks. For each individual entering the lick, we hand-recorded

species identity, time of arrival and departure, and activity during the visit.

Examining Tracks

On average, 8 licks (range 5 to 13) were checked for tracks every month from

January to November 2001, except in June (when only 1 lick was checked) and August

(when I was absent from the study site) (Table 2-1). We used this method to determine

the proportion of licks used every month by large terrestrial species. When the same lick

was checked for tracks more than once in the same month, we only used data for the first

day of checking. Species identity was established from the animals' tracks. Only fresh

tracks inside the licks were recorded at the time of checking. This method is not suitable

for arboreal animals (birds and arboreal mammals), and smaller terrestrial mammals

(such as pacas and agouties); they are likely to be underrepresented, especially when

other larger animals step on the same entrance paths.

Data Analyses

Lick visitors

An inventory of lick visitors was obtained by combining data from the three

detection methods (camera trapping, direct observation and tracks).

Frequency of natural-lick use

Data from camera traps, direct observations and tracks were analyzed separately to

describe the use of natural licks by wildlife species.

Camera traps. Frequency of lick visitation, as shown by camera trapping, was

estimated as the number of captures (photos) per 100 trap-nights (trapping success). A









trap-night is defined as each 24-hour period in which cameras were operational. Overall

trapping success was compared among species for the whole study period.

Direct observation. Frequency of lick visitation for each species (as shown by

direct observation) was estimated as the number of sightings per 100 h of observation

(sighting rate). Overall sighting rates were compared among species for the whole study

period. Comparisons were done separately for bird and mammal species. Among

mammals, comparisons were done for diurnal and nocturnal species separately. Also, for

species with more than 10 observations, comparisons of lick visitation rates among

seasons were done. Although, as mentioned above, seasonality in the study area is not

strong (a true dry season does not occur), the differences in rainfall and river levels led us

to define three seasons: heavy rainy season (from February to May), low rainy season

(from June to September), and moderate rainy season (from October to December). Since

the sampling effort was not exactly the same for each season (Table 2-2), for each

analyzed species, the expected frequency of lick visits was estimated by multiplying the

total number of visits by the proportions of sampling effort from each season (weighted-

count).

Tracks. For species detected with this method, the monthly rate of track

occurrences was estimated as the ratio between the number of licks with tracks present

over the total number of licks checked every month.

Within each data set (camera trapping and direct observation), comparisons of lick

visitation rates among species and/or among seasons were done with chi-square

goodness-of-fit tests. For all comparisons, ap-value <0.05 was considered significant.









When comparing only two categories (species), Yate's correction for continuity was used

(Zar 1974).

Lick-visitation rate and species abundance

To test the null hypothesis that wildlife species visit natural licks in proportion to

their abundance in the area, we used published information on abundance and density of

large mammals coming from a 1,827-km line transect censuses conducted in the Yavari-

Miri region from 1992 to 1999 (Bodmer et al. 2003, Salovaara et al. 2003). Data are

available for several primates, ungulates and large rodent species. A chi-square test of

homogeneity of proportions was used to compare the total number of sightings of

mammal species (using only direct observation data), relative to their density in the area.

Expected values for the test were obtained by multiplying the number of counts per

species by the proportion of their density in the area. Birds were not included in this

section because density data for most bird species are not available, except for large game

species (Begazo 1999).

Results

Lick Visitors

At least 7 species of birds and 15 species of mammals (a total of 21 species) were

detected at the licks by camera traps, direct observation and tracks (Table 2-3). Birds

found using the licks were medium to large species and included 1 species of rail, 1

species of curassow, 2 species of guans, 1 species of pigeon, and 2 species of parakeets.

Among mammals, lick visitors included 2 species of large primates, 4 species of

ungulates, 4 species of medium to large rodents, 2 species of cats (jaguar and ocelot), and

members of at least 2 families of bats. The cameras also captured a tail of an unidentified

mammal (possibly a bushdog), which was excluded from analyses.









Frequency of Natural-Lick Use

Camera traps

Sampling effort with camera traps totaled 412 trap-nights. That trapping effort

provided 87 photographs of animals at 14 natural licks from March to early December

2001. Photos recorded at least 17 species entering the licks (Table 2-3). Half of the

photographs (43) were bats captured at 2 licks (Table 2-4). Bats were common visitors in

most licks year-round (from direct observation). However, at the beginning of the study

we noticed that they excessively triggered the cameras, reducing the time cameras were

operational (on a single night a complete roll of film could be spent in only couple of

hours). Cameras were moved away from high bat-traffic areas, and thus bats may be

underrepresented in camera trapping for the rest of the year. Use of licks by bats is

mentioned in general, in the discussion below, but they were excluded from statistical

comparisons. Most bats at the licks were leaf-nose bats (Family Phyllostomidae), and at

least 23% of the bat pictures were of fruit bats (Subfamily Stenodermatidae).

Other than bats, the remaining 44 photographs showed 14 species visiting the licks

(Figure 2-2). The overall lick-visitation rate (detected by camera trapping) was not the

same across species (x2= 23.7, df= 13, p<0.05). These differences in lick visitation hold

when comparing only among mammals (2 = 15.5, df= 8, p<0.05), but do not hold when

comparing only among birds (x = 2.1, df = 4, p>0.05).

Excluding bats, lowland tapir (Tapirus terrestris) was the most frequent species

captured by the camera traps (10 photos in 412 trap-nights). Exclusive of pictures of the

same individual, at least 8 different tapirs were photographed at the licks. Tapir photos

come from 5 of the 14 licks sampled with camera traps, which are located in the middle

and upper Yavari-Mirin valley (Figure 2-1). Peccaries (Tayassu pecari and Pecari









tajacu), deer (Mazama americana), pacas (Agouti paca), and ocelots (Leopardus

pardalis) were captured 4 times at the licks, and the remaining species were registered

only 1-2 times with camera traps.

Direct observation

A total of 119 animals were detected at the 8 licks sampled from observation

platforms. Fifteen of the 21 species found at licks were seen with this method (Table 2-

3). Eighty-three animals were observed during day hours, and 36 animals were seen at

night (Table 2-5). Overall sighting rate was not equal across species (x = 88.3, df = 14,

p<0.05). Differences among species hold when comparing sighting rates among bird

species (x = 42.4, df= 5, p<0.05), and among mammal species (x = 42.5, df= 8,

p<0.05), separately. Among birds, pigeons (Columba subvinacea), parakeets (Pyrrhura

picta and Pionopsitta barrabandi), and blue-throated piping guans (Pipile cumanensis)

were the most frequent species at the licks, with sighting rates of 9.5, 4.7 and 4.3 sights

per 100 observation hours respectively (Figure 2-3.). Among diurnal mammals, black

spider monkeys (Ateles paniscus) were the most frequent visitors, with a sighting rate of

5.1 sightings/100 diurnal-observation hours. Howler monkeys and the two species of

peccaries and agoutis were seen also, but with less frequency (Figure 2-4.). Nocturnal

visitors to the licks were tapirs, pacas, red-brocket deer, and in one occasion a porcupine.

Red-brocket deer have both diurnal and nocturnal activity, but they were grouped within

the nocturnal mammals because they were seen at the licks only at night. Overall, tapirs

were the most frequent visitors to the licks across nocturnal species, with a rate of 3.8

sighthings/100 nocturnal-observation hours (Figure 2-5).









Examining tracks

A total of 24 licks were checked for tracks throughout the year. Tracks of lowland

tapir (Tapirus terrestris), white-lipped peccary (Tayassupecari), collared peccary

(Pecari tajacu), and red-brocket deer (Mazama americana) were found at the licks

almost all year-around (Figure 2-6). However, rates of track occurrences were higher for

lowland tapirs, except in January. Data from June, although it is displayed, is excluded

from this pattern because only one lick was checked for tracks that month. Track data

indicate that even though all ungulates use licks during the year, tapirs visit a higher

number of licks as compared to the other 3 species detected with this method.

Variation in Lick Use through the Year

Variation in lick use across the 3 seasons was determined only for the three most

frequently observed bird species (pigeons, parakeets and piping guans) and the two most

frequent mammals (spider monkeys and lowland tapirs). Although number of

observations seemed higher after June, that was the result of an increase in the sampling

effort. As a consequence, no significant differences were found when comparing the

number of sightings in proportion to the hours of observation across seasons for any of

the species tested (Table 2-6).

Lick-Visitation Rates and Species Abundance

Density estimations in the Yavari-Miri River valley were available for the

following mammalian species (Bodmer et al. 2003, Salovaara et al. 2003): spider

monkey (Ateles paniscus), red-hower monkey (Alouatta seniculus), lowland tapir

(Tapirus terrestris), white-lipped peccary (Tayassu pecari), collared peccary (Pecari

tajacu), red-brocket deer (Mazama americana), and black agouti (Dasyproctafuliginosa).

Comparisons among species indicate that these mammals did not visit the licks in









proportion to their abundances in the area (x= 795.15, df = 6,p<0.05). Three patterns

emerged from this comparisons: (a) species with low density and high visitation rate,

such as tapirs, spider monkeys and howler monkeys (Figure 2-7); (b) species with higher

densities and lower lick visitation rate, such as the 2 peccary species; and (3) species with

both low densities and low lick visitation rate, such as the red-brocket deer and the black

agouti (Figure 2-7).

Discussion

Lick Visitors

Birds. The Yavari-Miri region harbors a large diversity of birds (Lane et al. 2003).

The 7 bird species found visiting licks in the Yavari Miri River valley belong to 2

families of large birds (Rallidae and Cracidae) and 2 medium size birds (Columbidae and

Psittacidae). Among the large birds, the family Cracidae was the most common at the

licks. Three of the 4 species of Cracidae inhabiting the Yavari region (Crax salvini,

Penelope jacquacu and Pipile cumanensis) (Lane et al. 2003; Begazo 1999) were seen at

the licks, and represent 75% of the species of this family in the area. They are large birds

(>1.5 Kg) that use primarily interior forest habitats (Begazo 1999). Among the medium-

size birds visiting the licks, the most common (in fact the most frequent bird at the licks)

was the pigeon (Columba subvinacea), one of the 6 species of the family Columbidae

(16%) reported for this area (Lane et al. 2003). The other 2 bird species visiting the licks

were 2 species of parakeets (Pyrrhura picta and Pionopsitta barrabandi), which are

medium to small parrots, and account for the 10% of the parrot species reported in the

Yavari region (20 species) (Lane et al. 2003). Large parrots and macaws were not

observed at the licks, although they are reported using licks in other locations in the

Amazon. That is also the case for large parrots of the genus Amazona and at least 3









species of macaws (Ara several, A. chloroptera and A. macao), seen at a natural lick along

the riverbank of Manu River (Gilardi et al. 1999, Emmons & Stark 1979) and Madre de

Dios River (personal observation) in southern Peruvian Amazon. Most of these species

are present in the Yavari-Miri region (Lane et al. 2003, personal observation), but they

were not sighted in the licks studied. An explanation for their absence in those licks is

that large parrots are more common in open areas such as river pathways (Begazo 1999)

and above forest canopy (Gilardi & Munn 1998), while the licks studied were all found

more than 1 kilometer inside the forest. The high cliffs along riverbanks of several

Amazonian rivers, such as the Manu or Madre de Dios River, are not seen to the same

extent on the smaller Yavari-Miri River. In contrast, use of licks by the Cracidae (guans)

seems less common in the riverbank licks, than in the interior licks studied. This is

expected since those cracid species prefer interior forest (Begazo 1999).

All bird species observed at the licks were engaged in geophagy, but the reasons for

this behavior are not well understood. The several hypotheses proposed to explain

geophagy in birds have been examined for parrots (Gilardi et al. 1999), with evidence in

favor of the detoxification hypothesis, and secondary, the mineral supplementation

hypothesis. No information is available for the other bird species in regard to geophagy.

However, all the species at the licks have in common that they are frugivore (parakeets)

or frugivore/omnivore (Stotz et al 1996), and may use licks for similar reasons.

Independent of the specific benefits for the species, licks seem important for at least

a set of large and medium bird species in the Amazon. Those species, especially the

cracids, although less diverse than other bird groups, constitute a significant part of the









standing biomass of bird communities in the Neotropics (Terborgh 1986), and are

important seed dispersers (Levey 1994).

Mammals. The Yavari region is also home for a large diversity of mammals;

probably the highest recorded in any Amazon location, and possibly even the entire

Neotropics (Valqui 2001, Bodmer et al 2003, Salovaara et al 2003). Among the

mammals, the most common lick visitors were 2 species of primates, along with most

ungulates and large rodents. Although 13 species of primates exist in the Yavari-Miri

valley, most of them are medium to small size primates, and only 3 species are large

primates: the red-howler monkey (Alouatta seniculus), black spider monkey (Ateles

paniscus), and the wooly monkey Lagothrix lagothricha). Except for the latter, the

largest primates were the ones seen at the licks in this study. Although wooly monkeys

are mentioned in one study as lick users (Bicca-Marquez & Calegaro-Marquez 1994),

and at the study area were seen close to the licks on many occasions, they never actually

came down to eat soil, as observed for howler and spider monkeys. Smaller primates such

tamarins have been also reported eating soil (Heymann & Hartmann 1991), but more

from termite mounds than natural licks. Several species of howler monkeys and spider

monkeys also are reported regularly visiting licks in other tropical forest of Colombia

(Izawa 1993), French Guiana (Julliot & Sabatier 1993) and Brazil (Bicca-Marquez &

Calegaro-Marques 1994). Ateles paniscus is a frugivoros primate, while Aloutta seniculus

is more folivore species, although it includes fruits and other food items in its diet. In

general, no single reason for geophagy in primate species has been found (Krishnamani

& Mahaney 2000), or for these two genera of large Neotropical primates in particular









(Isawa 1993, Souza et al. 2002), but all hypotheses suggest nutritional or medicinal

benefits.

All ungulates living in the Yavari-Miri valley were seen at the licks, except for the

gray-brocket deer (Mazama gouazoubira). Local inhabitants, however, report that this

species is also a lick visitor, but their lower abundance compared to the other ungulates

may explain why they were not detected during the study period. Deer and tapirs are

browser/frugivore (Bodmer 1989), collared peccaries are frugivore/omnivore, and white-

lipped peccary are omnivore. Among rodents, the 2 large terrestrial rodents (paca and

agouti) and one arboreal species (porcupine) use licks. The terrestrial rodents (paca and

agouti) are also frugivores, and the arboreal one (porcupine) is a herbivore/frugivore. For

ungulates it is suggested that use of licks is related to their nutrition or heath. The

nutritional benefit hypothesis is examined in Chapter 3 and 4 for lowland tapir. Use of

licks by other South American ungulates also is reported in other locations. For example,

the Chacoan peccary also regularly visits licks (Sowls 1997), although its diet differs

somewhat from the Amazonian species (Taber 1993).

Other mammalian lick visitors were bats, mainly fruit-eating bats. These species

were very common all year-around at the licks. Little is known about the use of natural

licks by fruit bats. Some information is available on bat mineral nutrition, but mainly for

the Old World bats (Nelson 2003). Potential nutritional benefits could be expected for the

fruit-bat species observed in this study, and deserves more attention in future research.

The family Phyllostomidae is the most diverse and common in the Neotropics, and a

substantial number of species are fruit-eating bats. Their role in the tropical forest as seed

disperser is well known (Fleming 1988).









Other than primary consumers at the licks, carnivores such as jaguars (Panthera

onca) and ocelots (Leoparduspardalis) were also detected visiting these sites. There is

no record of any carnivore eating soil, and the purpose of their visits is probably related

to their prey, rather than a direct use of the soils at the licks. Jaguars eat a variety of prey,

including peccaries, pacas, agouties, and deer among other animals (Emmons 1987;

Sunquist & Sunquist 2002). Ocelots eat smaller prey, weighing less than a kilogram such

as spiny rats (Proechimys spp.). Also, although not prominent in their diet, ocelots may

occasionally kill agouties, deer and peccaries (Sunquist & Sunquist 2002). All these prey

species are lick visitors which may offer an opportunity for easy hunting to these

predators.

In summary, a relatively large group of mammalian species and large bird species

are lick visitors. Most of them are frugivore or frugivore/herbivore species, and may

obtain different benefits from the licks. Indirect benefits for non-herbivorous species are

proposed for carnivores, since they may reduce their cost of foraging, by visiting the licks

where prey may be concentrated. As a consequence, the use of licks also represents a cost

for their herbivore users, since the risk of predation is high inside the licks. All these

factors reveal that licks are an important component of Amazon forest for a relative large

number of species, and across the food guilds.

Frequency of Lick Use

From all the three method used in this study, the consistent pattern regarding

differences in licks visitation rate indicate that lowland tapir and spider monkeys, among

mammals, and pigeons, parakeets and guans, among birds, are the most frequent lick

users. No seasonality was found in their use of licks. This result contrasts with more

seasonality in lick use reported in other sites, such as eastern Brazilian Amazon (Ayres &









Ayres 1979) and southern Peruvian Amazon (Montenegro 1998). Those sites are clearly

more seasonal in terms of rainfall where differences between dry and wet season are

stronger. Compared to those other sites, the Yavari-Miri River valley showed lower

visitation rates, at least for species with some information. For example, at the Madre de

Dios River in Southern Peruvian Amazon, where seasonality is very strong, a very high

visitation rate to the licks was recorded for lowland tapir during the dry season

(Montenegro 1998), and red-brocket deer (Montenegro, unpublished data). In that study,

almost 200 observations of lowland tapir were obtained in about 3 months, whereas in the

Yavari-Miri valley, just over 20 direct observations were recorded during almost a year.

Several factors may explain these differences. Besides the differences in seasonality, at

the Madre de Dios River, the location of the study was at an ecoturism site where tapirs

were already habituated to human presence. At the Yavari-Miri River, tapirs were in

general more difficult to see, and the higher number of sightings occurred at those licks

further inside the forest. Also, although hunting it is slight compared to other locations in

Peru, licks are one of the preferred sites to hung tapirs (Chapter 5). Tapirs in the Yavari-

Miri valley seem to be more cautious when visiting licks, and may even return to their

trail before entering a lick when an observer is present. This behavior depends on the

individual, and is probably influenced by the previous experience of tapirs at licks used

by hunters.

Despite these differences, the common pattern in licks observed at Yavari-Miri and

Madre de Dios Rivers, is the relatively high number of lick users, with a higher visitation

rate by the lowland tapir, over other species. Spider monkeys also used licks in Madre de

Dios, but they seemed to prefer another lick, and since only one lick was regularly









monitored in that site, comparisons with Yavari-Miri are difficult. In summary, the most

frequent lick visitors overall are the lowland tapirs, and their use of licks is constant

through the year in the Yavari-Miri region.

Lick-Visitation Rate and Species Abundance

Wildlife species in the Yavari-Miri region did not use licks in proportion to their

abundance. Lowland tapirs had the lowest density, and yet, were the most frequent lick

visitors. Low density but high lick use was also observed by the spider monkeys and

secondarily by howler monkeys. Interestingly, peccaries are very abundant in the area,

especially white-lipped peccary, and even though peccaries use the licks, they do it with

less frequency compared to tapirs. White-lipped peccaries seem to perceive their habitat

at a different scale than collared peccaries (Fragoso 1998, 1999). They might be using

other licks, located farther away in the forest.

Overall, natural lick visitors comprise a relatively large set of species. The most

frequent visitors, both birds and mammals, are mainly large species that comprise a

substantial part of the standing biomass in the Amazon forest. Many of them are

frugivores or frugivore/herbivores that play an important role in the forest structure

through seed dispersion. Although the benefits for the species may vary, licks are an

important resource for a large number of species, and should be considered an indicator

of habitat quality for those species, and a key element in western Amazonian forests

Summary and Conclusions

A relative large number of Amazonian animals visit natural licks in the Yavari-Miri

River valley, in the northern Peruvian Amazon. Most species were large birds and

mammals. The most frequent species visiting the licks was the lowland tapir. No strong

seasonality in lick use was observed in the study area, as seems to occur in other tropical









forest. Species did not visit licks in proportion to their abundance in the area. Lowland

tapirs have low density compared to the other ungulates in the Yavari-Miri River valley,

and yet, they were the most frequent visitor of natural licks.

Table 2-1. Sampling effort used in three detection methods to determine the frequency of
natural-lick use by wildlife in the Yavari-Miri River Valley, during year 2001.

Camera Direct observation2 Examining
Month 1 3
trapping1 Diurnal Nocturnal Tracks

January --- --- --- 5.0
February --- 2.0 38.0 7.0
March 29.0 8.0 61.0 7.0
April 1.0 5.5 0.0 6.0
May 7.0 5.0 73.0 11.0
June 9.0 12.5 24.0 1.0
July 21.0 36.5 60.0 9.0
September 108.0 64.0 84.0 6.0
October 141.0 49.0 72.0 10.0
November 98.0 62.0 120.0 13.0
December 2.0 7.5 12.0 ---
Total 412.0 252.0 544.0 24.04
1 Number of trap-nights (number of 24-hour periods when cameras were operational).
2 Number of hours spent at observation platforms.
3 Number of licks checked for tracks.
4 Cumulative number of licks checked at the end of the study period.

Table 2-2. Sampling effort used in direct observation per season.

Direct observation
Season
Day (h) Night (h)
Heavy rainy (Feb-May) 21 172
Low rainy (Jun-Sep) 113 168
Moderate rainy (Oct-Dec) 118 204

Total 252 544


h = cumulative hours of observation.










Table 2-3. Species detected at natural licks by camera trapping, direct observations and
tracks in the Yavari-Miri River valley, Peruvian Amazon.


Species

BIRDS
GRUIFORMES
Family Rallidae
Aramides cajanea
CRACIFORMES
Family Cracidae
Crax salvini
Penelope jacquacu

Pipile cumanensis
COLUMBIFORMES
Family Columbidae
Columba subvinacea
PSITTACIFORMES
Family Psittacidae
Pyrrhura picta
Pionopsitta barrabandi
MAMMALS
CHIROPTERA
Subfamoly.
Stenodermatidae
Other Phyllostomidae
PRIMATES
Family Cebidae
Alouatta seniculus
Ateles paniscus
CARNIVORA
Family Canidae
Speothos venaticus*
Family Felidae
Leopardus pardalis
Panthera onca
PERISSODACTYLA
Tapirus terrestris
ARTIODACTYLA
Family Tayassuidae
Tayassu pecari
Pecari tajacu
Family Cervidae
Mazama Americana


English name


Grey-necked wood-rail


Salvin's curassow
Spix's guan
Blue-throated piping-
guan


Ruddy pigeon


Painted parakeet
Orange-cheeked parrot



Fruit-bats
Bats


Red howler monkey
Black spider monkey


Bushdog

Ocelot
Jaguar

Lowland tapir


White-lipped peccary
Collared peccary


Local name


Camera Direct
Tracks
traps observation


Paujil
Pucacunga

Pava negra


Paloma


Lorito
Lorito


Mashu
Mashu


Coto
Maquisapa


Tigrillo
Otorongo

Sachavaca


Huangana
Sajino


Red-broket deer Venado rojo


x x










Table 2-3 (continued)
Camera Direct
Species English name Local name r Tracks
traps observation


RODENTIA
Family Erethizontidae
Coendou prehensilis
Family Agoutidae
Agouti paca
Family Dasyproctidae
Dasyproctafuliginosa
Family Echimidae
Proechimys sp.
* Probable.


Porcupine


Paca


Black agouti

Spiny rat


Table 2-4. Number of monthly photo-captures at 14 licks form March to December 2001,
in the Yavari-Miri River Valley, Peruvian Amazon
Season


Heavy rainy
Mar Apr May


Low rainy
Jun Jul Sep


Moderate rainy
Oct Nov Dec


BIRDS
Aramides cajanea
Crax salvini
Penelope jacquacu
Pipile cumanensis
Columba subvinacea


MAMMALS
Subfamiliy Stenodermatidae
Other Phyllostomidae
Leopardus pardalis
Panthera onca
Tapirus terrestris
Tayassu pecari
Pecari tajacu
Mazama Americana


3 1
1
1 4 3 1
4
1 1
2 2


Agouti paca 4 4
Dasyproctafuliginosa 1 1
Proechimys sp. 1 1
Number animal photos 24 0 0 0 1 30 14 17 0 86
Trapping effort (# trap-nights) 29 1 7 9 21 108 141 94 2 412


Erizo

Majas


Afiuje

Sachacuy


Species


Total










Table 2-5. Frequency of birds and mammals observed at eight natural licks from
February to early December (excluding August), 2001 in the Yavari-Mirin
River Valley, Peruvian Amazon.


Time of observation/Species

Day
Birds
Crax salvini
Penelope jacquacu
Pipile cumanensis* (1-5)
Columba subvinacea
Pyrrhura picta* (>50)
Pionopsitta barrabandi*
(>20)
Mammals
Alouatta seniculus* (5)
Ateles paniscus* (2-3)
Tayassu pecari* (>50)
Pecari tajacu* (2)
Dasyproctafuliginosa
Diurnal sightings/month
Day hours/month
Sighting rate
(Sights/day hours)


Feb Mar Apr May


Jun Jul Sep Oct Nov Dec Totals


2.0
4.0
5.0 5.0
1.0 5.0


1.00


1.00 1.0
1
2.0 0.0 1.0 5.0 9.0
8.0 5.5 5.0 13.0 36.5


2
2.0 4
8.0 4
3.0 2


1.0 1.0 3
5.0 5
1.0
1.0
2.0 1.0
21.0 22.0 2(
64.0 49.0 62


1.5 0.2 0.0 0.2 0.4 0.25 0.33 0.45


1.0
5.0
12.0
24.0
11.0


5.0
13.0
4.0
3.0
4.0
0.0 83.0
7.5 252.0


0.32 0.0 0.33


Nigth
Mammals
Tapirus terrestris
Mazama Americana


2.0 3.0 2.0
1.0


4.0 4.0
1.0 1.0


5
1


Agoutipaca 1.0 3.0 2.0 1.0 1.0
Coendou prehensilis 1.0
Sightings per month 2.0 6.0 0 5.0 3.0 3.0 6.0 5.0 6 0.0
Day hours/month 38.0 61.0 0 73.0 24.0 60.0 84.0 72.0 120 12.0
Sighting rate (sights/night
Hours) 0.05 0.1 0 0.07 0.1 0.05 0.07 0.07 0.05 0.0
Total sightings
Total observation hours
Overall sighting rate (total sights/total
Hours)
* Sightings of groups, not individuals (group size in parenthesis).


21.0
6.0
8.0
1.0
36.0
544.0

0.07
119.0
796.0

0.15











Table 2-6. Chi-square values for testing the null hypothesis that number of sightings is
the same in the three seasons.


Species
Birds
Columba subvinacea
Pyrrhura picta
Pipile cumanensis
Mammals
Ateles paniscus
Lowland tapir


2.194
1.152
0.053

5.037
3.131


p-value


>0.05
>0.05
>0.05

>0.05
>0.05


.~n J




U
U


a


4





A


Natural licks
A/ Rivers.

Geomorphological units
Flood Plain
Sedimentary Plain
Terraces


+ 3000
Vp


0 3000


Figure 2-1.Location of 24 natural licks found in the Yavari-Miri RiverValley,
northeastern Peru.


6000 Miles













Tapirus terrestris
Tayassu pecari
Mazama americana
Agouti paca
Leopardus pardalis
Pecari tajacu
Panthera onca
Dasyprocta
Proechimys sp.

Columba cayannensis
Pipile cumanensis
Penelope jacquacu
Aramides cajanea
Crax salvini


Mammals






-Birds


1 1.5 2 2.5


Photo-captures/100 trap-nights

Figure 2-2.Photo-captures per 100 trap-night per species at 14 licks from March to
December 2001 in the Yavari-Mirin River Valley, Peruvian Amazon
(excludes bats).


Columba subvinacea
Pipile cumanensis
Pyrrhura picta
Penelope jacquacu
Pionopsitta barrabandi
Crax salvini


0 2 4 6 8 10
Sighting rate
(Sights/100 diurnal-observation hours)

Figure 2-3. Total sighting rate of bird species at 8 licks surveyed from February to early
December 2001 in the Yavari-Miri River Valley, Peru.


0 0.5











Ateles paniscus

Alouatta seniculus


Dasyprocta fuliginosa


Tayassu pecari


Pecari tajacu


0 1 2 3 4 5 6

Sighting rate
(Sights/100 diurnal-observation hours)


Figure 2-4. Total sighting rate of diurnal mammal species at 8 licks surveyed from
February to early December 2001 in the Yavari-Miri Valley, Peru.





Tapirus terrestris


Agouti paca

Mazama americana


Coendou prehensilis


0 1 2 3 4 5

Sighting rate
(Sights/100 nocturnal-observation hours)


Figure 2-5. Total sighting rate of nocturnal mammal species at 8 licks surveyed from
February to early December 2001 in the Yavari-Miri Valley, Peru.










Tapirus terrestris
O Tayassu pecari
Pecari tajacu
t OMazama americana


Jan Feb Mar Apr May Jun Jul Sep Oct Nov


Figure 2-6. Ratio of track occurrences for tapir (Tapirus terrestris), white-lipped peccary
(Tayassupecari), collared peccary (Pecari tajacu), and red-brocket deer
(Mazama americana) from January to November of 2001 in the Yavari-Miri
Valley, Peruvian Amazon.


O Density
* Sighting rate


0.04 |

0.03

0.02 .2


Figure 2-7. Density of selected mammals in the Yavari-Miri River valley and their
overall lick-visitation rate during year 2001.


0.6
0.4
0.2
0


.~ -z
~


rmH


kl


F-I














CHAPTER 3
NATURAL LICK SOILS AS SOURCE OF MINERALS FOR WILDLIFE IN THE
YAVARI-MIRI REGION

Introduction

Soils indirectly influence nutrition of herbivores through the amount and quality of

plant biomass they produce. However, since many animals purposely consume or lick

soil materials (a behavior known a geophagy), a more direct effect of ingested soils is

also considered (McDowell 2003). Many wildlife species engage in geophagy, and

diverse studies link this behavior to their mineral nutrition (Hebert & Cowan 1971;

Weeks & Kirkpatrick 1976; Robbins 1983; Stark 1986; Jones & Hanson 1985; Klein &

Thing 1989; Moe 1992; Kennedy et al. 1995; Tracy & McNaugthon 1995; Holdo et al.

2002). Other researchers, however, associate soil ingestion with the potential benefits of

clay in soils, such as buffering gastrointestinal fluids (Oates 1978), avoiding diarrhea

(Mahaney 1993; Mahaney et al. 1996; Mahaney et al. 1997), or providing protection

against toxic plant secondary compounds (Gilardi et al 1999). The latter two benefits

have been suggested due, in part, to a higher content of clay of some geophagical soils as

compared to non-consumed soils.

Geophagy is usually selective, occurring in specific locations commonly termed

natural, mineral, salt or clay licks, depending on the benefits attributed to soil

consumption. Characterization of soils from natural licks is available for several sites of

North America (Jones & Hanson 1985; Kennedy et al. 1995; Tracy & McNaughton

1995). In the tropics, chemical features of licks are available for Old World tropical









savanna habitats (Weir 1972; Ruggiero & Fay 1994; Holdo et al. 2002), and to a lesser

extent, for tropical forest sites (Klaus et al. 1998; Moe 1993). In the Amazonian

Neotropics, natural licks have been characterized for a few sites, such as southern Peru

(Emmons & Stark 1979; Gilardi et al. 1999), a site in Brazil (Ayres & Ayres 1979) and

southeastern Colombian Amazon (Narvaez & Olmos 1990; Lips & Duivenvoorden

1991).

Results from the above studies vary, and comparisons are difficult because of

differences in methods (including chemical determinations), number of natural licks

sampled, presence/absence of control samples and their collection site with respect to

licks, types of licks studied, geographical location, animal species using the licks, and

general research questions, among others. Also, natural licks around the world have

different origins and characteristics, and the benefits to wildlife are obscured by regional

differences in soil properties. For these reasons, it is necessary to consider not only the

chemical composition of the licks, but their geoecological context in order to better

interpret their role in the ecology of their users.

In tropical areas with high rainfall, some elements are easily leached and usually

pose a challenge for the mineral nutrition of many wildlife species (Robbins 1983). One

of the regions where such limitation exists is the Amazon basin, where precipitation is

high, ranging 2000-3000 mm annually (Marengo 1998). Most of the Amazon forest is

characterized as having very acid soils, low in available nutrients, and high in

concentrations of toxic Al. In this type of environment, herbivore species may face

mineral limitations if their only source of minerals is the plant resources. If natural licks

in the Amazon region provide some minerals of nutritional importance for herbivores,









they might play an important role in animal nutritional ecology and population

persistence.

A region in the Amazon where natural licks occur and where many species persist

in healthy populations is the Yavari-Miri River valley, in northeastern Peru (Salovaara et

al. 2003). A relatively high number of wildlife species use natural licks in the Yavari-

Miri River valley (Chapter 2), including all resident ungulates (especially lowland tapirs),

two species of monkeys, large rodents and large birds. It is unknown whether all these

species are attracted to the licks for the same reasons. However, it is thought that for the

herbivores in particular, licks might provide some elements of nutritional importance.

Also, it might be that those licks provide other, not necessarily exclusive, benefits to the

animals, such as clay, as suggested for other Amazonian licks (Gilardi et al. 1999).

The purpose of this chapter is to describe the natural licks occurring in the middle

Yavari-Miri River valley of the Peruvian Amazon in terms of their size and location

along the river, and to evaluate them as a source of minerals and/or clay for Amazonian

herbivores. The hypotheses examined in this study were the following:

* Hypothesis 1. Soils at natural licks have higher mineral concentration (for one or
more minerals) than non-lick soils.

* Hypothesis 2.There is no difference in soil mineral content between high water and
low water seasons.

* Hypothesis 3. Lick soils have higher clay content as compared to non-lick soils.


It is predicted that if natural licks in the Yavari-Miri River valley are a direct source

of minerals, higher concentrations of one or more extractable elements will occur in lick

soils as compared to non-lick soils. Also, if natural licks are a reliable source of minerals

through the year, it is predicted that their mineral concentrations (at least for some









elements) do not substantially drop throughout the year. Also, if animals are attracted to

the licks for their clay content, it is predicted that higher percentages of clay content will

differentiate lick form non-lick soils. To test these predictions comparisons of several

physical and chemical characteristics of lick and non-lick materials were conducted and

analyzed within the regional geo-ecological context.

Study Site

The study was conducted along the Yavari-Miri River, a tributary of the Yavari

River, in the Department of Loreto, in northeastern Peru. Fieldwork was conducted

throughout the middle course of the Yavari-Miri River, in the area between 4o30.23'S,

7226.69W and 4o24.77'S, 7209.76'W. This area is located from San Cristobal Creek

upstream to Maquisapay Creek (Figure 3-1). Elevation in the area covered in this study

varies from about 90 to 120 meters above see level. Mean annual temperature in the

region is 26C, with monthly mean maximum temperatures ranging from 28 to30C, and

monthly mean minimum from 17 to 20C. Mean annual precipitation ranges from 2400 to

3100 mm (Marengo 1998), with the highest monthly rainfall occurring from February to

April (as high as 350 mm), and the lowest from June to September (as low as 180 mm).

In spite of these monthly differences, there is no real dry season, as occurs in more

southern regions of the Peruvian Amazon. Monthly rainfall differences are, however,

reflected in the Yavari-Miri and Yavari river water levels and discharge. The water levels

are the highest during the months of heavy rainfall (February to April), and this period

will be called here the high water season. The lowest water level of the Yavari-Miri River

occurs during the months of less rainfall (June to September), when sand beaches appear

along some riverbanks. The Yavari-Miri is a black water river relatively narrow, and









could appear very shallow during the least rainy months. This latter period will be called

here the low water season.

Geology of the Yavari-Miri valley is not known in detail, but research conducted

around the Iquitos area (Rasanen et al. 1998), and along the Amazon River (Hoorn 1993)

provides useful regional information. The main geological formation in the area is the

Pebas formation, a thick layer of sediments covering a large area of northern Peru, and

equivalent to sediments of northwestern Brazil and southeastern Colombia (Hoorn 1993).

The area is also associated with the Iquitos Arch, an uplifted geological structure that

separates the Amazon and Marafion Sedimentary basins (Hoorn 1993).

The three main geomorphic units in the study area are terraces, alluvial plains and

sedimentary surfaces (Figure 3-1). Main habitat types in the area are upland forests and

flooded forests. Upland forests cover most of the area, and exist on terraces and

sedimentary surfaces. They are not uniform throughout the area, but change in plant

composition because of soil heterogeneity, somewhat similar to the upland forest around

Iquitos (Ruokolainen & Tuomisto 1998; Pitman et al. 2003). Flooded forests exist on the

alluvial plains of the Yavari-Miri and Yavari rivers. Swamp forests, a type of flooded

forest, are common along these rivers, covering 25 to 50% of the flood plains (Pitman et

al. 2003), and occur also on poorly drained upland soils.

Plant and animal diversity in the area is very high (Pitman et al. 2003). The high

mammalian species richness leads some to consider the Yavari valley as one of the

mammalian diversity hotspots in Peru (Valqui 1999, 2001; Salovaara et al. 2003).

Although there is some hunting in the area, it is slight compared to other sites in the

Peruvian Amazon (Bodmer & Puertas 2000; Bodmer et al. 2003), and many wildlife









species are still abundant. Lowland tapirs and other ungulates, for instance, have healthy

populations at the Yavari-Miri River (Salovaara et al. 2003).

Methods

Lick Location and Description

From January to March 2001, an intensive search for natural licks was conducted

along 66 km in trails on both sides of the Yavari-Miri River. Trails were cut across the 3

landscape units of the area (flood plains, terraces and sedimentary surfaces), and across

an area of approximately 220 km2. This search yielded 21 natural licks. Three additional

licks were found in July during a parallel research project at the Yavari-Miri River

(Salovaara, in prep.), for a total of 24 licks found from the San Cristobal Creek to

Maquisapay Creek. Once a natural lick was found, its geographical coordinates were

taken with a global positional system (GPS), and marked on a 1:100,000-scale map.

Licks were measured (length and width) and described in terms of their form,

number of geophagical sites (spots where animals eat soil) and general features of

vegetation cover. Location of licks was displayed on top of a satellite image of the study

area using the software ArcGIS to determine their distance to the river and the

physiographic unit where they occurred.

Physical and Chemical Characterization of Lick Soils

Soil sampling

Soil samples from 7 licks were collected both during the high water season (March

- April), and the months of low rainfall or low water season (September-October). At

each lick, 1 to 2 composite samples were collected from the sites where animals ate soil,

plus a composite control sample from areas within 10 to 20 m outside of each lick. Each

composite sample was made up from 3 to 4 sub-samples. Additionally 6 licks were









sampled (lick and nearby non-lick soils) in September through November 2001, for a

total of 13 natural licks sampled in those months. For the whole year, a total of 55

samples was collected (35 lick soil samples and 20 control samples, Table 3-1). Each

sample (about 1 kg) was air dried and stored for further analysis. All natural licks

sampled also were monitored for animal activity with one or several methods (Chapter 2).

Laboratory analyses

Samples were sent for analysis to the Terrapreta Soil Laboratory, a private

laboratory in Colombia. Chemical characterization of soils was conducted using the

methods described by IGAC (1990), and included the following: soil texture, pH, organic

C, available P, exchangeable Al, carbonates (CO3), cation exchange capacity (CEC), and

extractable Ca2+ Mg2+, K and Na Samples collected during the high water season also

were analyzed for concentration of B, Cu, Fe, Mn, Zn and S. Percentages of sand, silt and

clay in soil samples were determined by the Bouyoucos hydrometer method. Soil pH was

measured with a potentiometer in a volumetric 1:1 soil: water suspension. Organic carbon

was determined by the Walckley-Black method, which uses chromic acid to measure

oxidisable organic carbon in soil (Walkley & Black 1934; IGAC 1990). Available P was

measured with the Bray II method, in which P is extracted using Bray II solution and

measured colorimetricly, based on the reaction with ammonium molybdate (Bray &

Kurtz 1945; IGAC 1990). Exchangeable Al was determined by the Yuan's method in

KCl extractions (Yuan 1959; IGAC 1990). Carbonate concentration was qualitatively

measured by reaction with 10% HC1. Cation exchange capacity and exchangeable Ca2

Mg2+, K and Na+ were extracted with IN ammonium acetate at pH = 7. B, Cu, Fe, Mn,

Zn and S were extracted with acid solutions of HCL and H2SO4. Concentrations of these

elements in extracts were determined by atomic absorption spectrophotometry.









Data analysis

Since samples from each lick were matched with non-lick samples from nearby

areas, differences in element concentrations between lick and non-lick samples were

tested within seasons using paired t tests (Zar 1974). Likewise, differences in element

concentrations between high water and low water seasons were tested with paired t tests,

using data from only those licks that were sampled in both seasons. For the latter tests,

comparisons were made among licks and non-lick samples separately. Since the paired t

test requires that differences among related samples have a normal distribution, a test for

normality was conduced for each data set using the Kolmogorov-Smirnov test for

normality. All tests for normality were non-significant, and no data transformations were

needed to reach normality. For all tests, ap-value <0.05 was considered significant. All

statistical analyses were performed with the software SPSS version 11.5 for Windows.

Results

Lick Location and Description

Most natural licks found at the Yavari-Miri River, between San Cristobal Creek to

Maquisapy Creek, where located in the area on the northwest side of the river. Only 1

natural lick (lick number 14) was located on the right side of the Yavari-Miri River, on its

flood plain. Distance to the licks from the river varied from 0 m (at the river bank) to

5,400 m in the upland forest (Table 3-2). Licks were located at elevations varying from

92 116 m. The majority of licks (18 or 75%) were located on the sedimentary plain, and

the remaining 6 (25%) were located on the Yavari-Miri River flood plain (Table 3-2,

Figure 3-1). No lick was found on terraces.

Natural licks were classified according to their location as the following 4 types:

(1) upland licks, (2) low bajial licks, (3) high bajial licks, and (4) river bank licks.









Upland licks (n = 18) were located on the sedimentary plain, in an upland forest

environment that does not flood at any time of the year. These licks occur in forest

openings, usually in depressions 3 10 m deep, often with large stones, and caves made

by constant mining of the animals. Numerous animal teeth marks on the carved holes are

present, and are accessed by clear animal paths. Most of these licks are close to small

creek headwaters. Vegetation cover inside these licks is scarce, represented by some palm

trees, shrubs and some ferns scattered on muddy surfaces. Low bajial licks (n = 2) were

located on low flooded plains that are inundated for several months during the high water

season. They were located in low areas with poor drainage, from a few up to 400 meters

away from the riverbank. This type of lick is functional only during the drier months of

the year (June to September), and even in those months, may become flooded for several

days after a heavy rain. Vegetation inside those licks is mainly herbaceous with scattered

bushes on a muddy, soft surface. High bajial licks (n = 3) were also located on the

flooded plain of the Yavari-Miri River, but unlike low bajial ones, they are flooded for

shorter periods of time (approximately 30-40 days a year). They were located from 161 to

436 m from the riverbank (Table 3-2). Finally, 1 riverbank lick was found on the Yavari-

Miri River. Although a few more licks of this type exist along the Yavari-Miri River,

they were difficult to identify because they are underwater for several months of the year,

and animal paths usually disappear with the flooding.

Lick size varied from 10 m2 to 1,196 m2. Total area of licks added up to 7,282 m2.

Total area of these licks represents 0.0033% of the 220 km2 crossed by the trails.

Although it is possible that some licks were missed in the search, their proportional area

is very small. Number of geophagical sites inside the licks varied from 1 to 3 depending









on the size and form of the lick, with the largest licks having more than one geophagical

site.

Physical and Chemical Characterization of Lick-Soils

Particle size

In lick soils, mean percentages of sand, silt and clay were 39.5 8.5 %, 41.5 +

6.9%, and 18.9 11.18%, respectively. In non-licks soils, proportion of sand, silt and

clay were 35 6.6%, 37.7 7.3 % and 27.22 7.6, respectively (Figure 3-2). Differences

between lick and non-lick soils regarding particle size proportions were not significant

(p>0.05). Texture of individual samples varied from loam to sandy loam, silt loam and

clay loam. All textures were found in both lick and non-lick soils. However, loam soils

were the most frequent across all samples.

Chemical properties of lick and non- lick soils

Soil pH was higher in lick samples as compared to non-lick samples (Table 3-3),

both in the high water season (t = 11.84, df = 6, p< 0.001), and the low water season (t =

7.74, df = 12, p< 0.001). In general, licks soils were either neutral or alkaline with a pH

of 7 to 8, whereas non-lick soils were always acid, with pH of 3.5 to 5.

Mean percentage of organic carbon varied from 0.6 0.27 % in non-lick soils to

1.26 1.03 % in lick samples (Table 3-3). Although organic carbon seems to be higher in

lick soils, there was a large variation within samples (range 0.3% to 3.7%), and

differences were not significant in either the high water (t = 1.18, df = 6, p = 0.28) or the

low water season (t = 1.82, df= 9, p = 0.10). However, most samples, from both lick and

non-lick soils had relatively low organic carbon, usually less than 1%.

Exchangeable Al was very low in lick samples compared to non-lick samples in

both seasons. In fact, only in the low water season, some free Al+3 was found in lick soils,









but in a much lower concentration than in non-lick soils (t = 4.16, df= 6,p = 0.009), and

none was found in the high water season (Table 3-3). In contrast, in non-licks soils,

exchangeable Al varied from 11.65 to 12.88 meq/100 kg of soil.

Cation exchange capacity varied on average from 21.88 4.32 to 25.22 5.76

meq/100 g of soil (Table 3-3), with no significant difference between lick and non-lick

soils either in the high water season (t = 0.78, df= 6,p = 0.46) or the low water season (t

= 1.59, df= 12, p = 0.13). Lick soils had higher base saturation (many times over

saturation) than non-lick soils (Table 3-3).

Lick soils had higher content of P, Ca, Mg, and Na than non-lick soils, and those

differences were consistent in both seasons (Table 3-3). Likewise, B, Cu, and S were

present in higher concentrations in lick samples as compared to non-lick samples (Table

3-4). No significant differences between lick and non-lick soils were found for K, Fe, Mn

and Zn concentrations (p>0.05, Tables 3-3 and 3-4). Comparing lick and non-lick soils

between seasons, concentration of Ca in lick soils increased during the low water season

(t = 6.4, df = 6, p = 0.001). Na concentration increased also during the low water season

in lick soils (t = 2.49, df= 6,p = 0.047), and marginally in non-lick soils (t = 2.40, df= 7,

p = 0.053), being always much higher in lick than non-lick samples (Table 3-3). No

seasonal differences were found for P, Mg and K concentrations (p>0.05) within each

soil type. No seasonal comparisons were done for concentration of microminerals (B, Cu,

Fe, Mn, Zn and S) because they were analyzed only in samples from the high water

season.









Discussion

Lick Location and Description

Location and other features of the natural licks at the Yavari-Miri River are related

to the geological formations, landforms, and past and present tectonic processes in the

area. Researchers often associate natural licks in this part of the Amazon with the Pebas

formation (Lips & Duivenvoorden 1991; Hoorn 1993). This formation is made of

sediments deposited during the Middle Miocene (11 tol7 million years) in a long lasting,

large shallow lake system with fluvial influence from the Andes, and occasional marine

incursions from the Caribbean (Hoorn 1993; Rasanen et al. 1998). The Pebas formation

is characterized by blue clay alternating with sand and lignite layers with an abundant

presence of fossil mollusks (Hoorn 1993).

From a satellite image of the area, it is noted that main rivers in this part of the

Amazon basin are controlled by a general linear pattern with a SW-NE orientation,

dissected by smaller rivers running in a NW-SE linear pattern. These alignments form a

tectonic micro-block pattern that indicates neotectonic activity. A similar pattern exists in

the southern Colombian Amazon (IGAC 1999). Because of this neotectonic activity, the

Yavari-Miri and Yavari Rivers are being "pushed up" in a NW direction. As a

consequence, terraces are formed to the SE of rivers, whereas on the NW side, the action

is mainly erosive. This dynamic could be related to fact that most licks were found on the

NW side of the Yavari-Miri River, where erosive activity is stronger. This fluvial erosion

is probably associated with some of the riverbank licks of the Yavari-Miri River valley

because it sporadically exposes the Pebas formation sediments.

Riverbank licks, as named in this study, coincide with the barranco (cliff) licks

described in the middle Caqueta region of southern Colombia, about 400 km north of the









Yavari-Miri River (Lips & Duivevoorden 1991). Also, some of the licks termed in this

study as upland licks could coincide with the abandoned meanders (Lips &

Duivenvoorden 1991), which are formed when old streams dissecting the sedimentary

plain become dry during low water season. This latter type of lick is probably formed by

a subterraneous flux of water enriched with elements leached form either sediments of

the Pebas formation or sediments of different origin. In fact, although most of the

sedimentary plain is characterized by low mineral content, superficial sediments can be

very variable, with some having higher nutrient contents, depending on many factors

(Linna 1993). Therefore, some licks may not be directly related to the Pebas formation,

but could be associated with the flux of enriched water leaching superficial sediments.

The names given to licks in this study (upland, high bajial, low bajial and

riverbank licks) reflect their location on the main landforms in the area, rather than their

origin. This classification is arbitrary, with the intention to reflect their functionality

through the year. Riverbank licks (especially if their location is within maximum-

minimum water level), as well as low bajial licks are functional only when they are

exposed, during low water season (from June to September-early October).

Upland licks are more permanently functional since they do not become flooded at

any time of the year. However, those licks are not static, but may occasionally lose their

function, when new sediments cover the exposed materials that attract the animals. This

dynamic, however, occurs on a larger time scale, and thus is difficult to monitor in the

short term. In the study area some old licks were found where the caves carved by the

animals are still evident, but with no sign of recent use, and even with growth of pioneer









plants. These considerations indicate that contrary to what it may seem, natural licks are a

dynamic resource.

Licks in the study area were relatively small, compared to licks in other sites of the

world, such those used by large mammals in Africa (Klaus et al. 1998) and Asia (Moe

1992). Licks in those parts of the world may actually be very large, which is associated

with the size and density of their users. The users of African licks, for example, are

elephants and large ungulates, some of which occur in high densities (Klaus et al 1998).

The Amazonian licks are not as impressive in size, because their users are not as large as

the African ones. However, in all these regions (Africa, Asian and the Amazon) the licks

occupy a small proportion of the habitat, but yet, are frequently used by many species. In

this study, all ungulates, and several species of large rodents, large primates and large

birds frequently use licks (Chapter 2), and even if they represent a small proportion of

their habitat, they appear to be a very important resource for these species in the Yavari-

Miri River valley. In other words, natural licks in the study site may play an important

role in the ecology of their users, disproportionately to the area they occupy.

Physical and Chemical Characterization of Licks

Particle size

Natural licks did not show significantly higher mean clay content as compared to

non-licks samples. This contrasts with findings in other licks of southern Amazonia in

which clay content was 50% vs 35% in non-lick samples (Galetti et al. 1999). In the licks

in the Yavari-Miri region, mean clay content was about 19% vs 27% in non-lick samples,

and the difference was not significant due to variation in both sets of samples. This

percentage of clay content is considered medium according to the scale (15 to 40%) used

by Kauffman et al. (1998) for the upland soils around Iquitos. Only 2 lick samples (out of









32) were classified as clay (about 40% of clay), and 5 were classified as clay loam (>28%

of clay). The same textures were present in non-lick samples. Also, in the licks studied in

the Colombian Amazon, 2 licks of the type called "abandoned meander" had high sand

content (68-86% respectively) (Lips & Duivenvoorden 1991). In addition, 2 of the 3 soil

samples consumed by mustached tamarins (Saguinus mystax) at the Rio Blanco, in

northeastern Peruvian Amazon, were sandy and only 1 was fine-grained (Heymann &

Hartmann 1991). Results of our study do not support the hypothesis that it is the clay

content that attracts animals to the licks, as may be the case for large parrots and macaws

at licks in southern Peru (Gilardi et al 1999). These results agree with the view that there

is not a single reason for geophagy across species. Most licks studied in the Yavari-Miri

River valley were located inside the forest, and large parrots or macaws were never

observed in those licks, although they were observed flying above the tree canopy and

along the Yavari-Miri River.

Chemical properties of lick and non- lick soils

Lick samples had the following differences with non-lick samples: higher pH,

minimum free aluminum, and higher content of P, Ca, Mg, Na, B, Cu and S. These

results coincide with other lick characterizations in the Amazon region, in which more

than one element is in a higher amount at the licks. For example, Ca, Mg, Na and

sometimes K have been frequently more abundant in natural licks of Manu, in southern

Peru (Emmons & Stark 1979; Montenegro 1998), middle Caqueta region of Colombia

(Lips & Duivenvoorden 1991), and Amacayacu, in southern Colombia (Narvaez &

Olmos 1990). In other tropical areas, like Africa, licks also show a high content of Na

(Weir 1972; Abrahams 1999; Holdo et al. 2002) and other elements, including Ca, Mg, P,

and some times K (Klaus et al. 1998; Ruggiero & Fay 1994; Hensahaw & Ayeni 1971;









Tracy & McNaugthon 1995). In a few cases, however, researchers have found it difficult

to determine differences between lick and non-lick soils because of the large variation

among samples (Seidensticker & McNeely 1975). An important factor in some studies

has been the nature and origin of control samples, which may obscure actual differences

of lick vs non-lick materials. Some times samples used as controls come from very

distant sites from the licks and the regional variation of soil properties is seldom taken

into account when doing comparisons.

In temperate areas, licks used by large ungulates are often rich in Na (Hebert &

Cowan 1971; Fraser & Hristienko 1981; Klein & Thing 1989, Tankersley & Gasaway

1983; Miller & Livitaitis 1992). However, at a large scale some differences occur across

the whole region. For example, in eastern North America the main elements in licks are

Na and Mg, whereas in western North America they are Ca and Mg (Jones & Hanson

1985).

Since often more than one element is in higher concentrations at the licks,

researchers find it difficult to attribute the use of licks to one single element as the one

sought by the animals. However, it is important to consider that availability of one

element in the soil is not independent to the other elements, as well as other properties of

the soil. For this reason, in order to better interpret the differences between lick and non-

lick samples found in this study, it would be useful to consider not only the high

concentration of some elements, but also other soil properties.

Differences among lick and non-lick soils in this study fit in several aspects the

characterization of 1 of 5 group soils described by Kauffman et al. (1998) for the upland

areas (terra firme) around Iquitos, 170 km west of the study site on the Yavari-Miri









River. This group of soils (group I in Kauffaman et al. 1998) are young soils, not or

slightly lixiviated, occurring on sites where erosion had exposed parental materials

unaltered with meteorizable minerals such those of the Pebas formation or the named

Buena Union unit (a unit described by the Amazon River, close to the Iquitos area). Such

soils are located in low areas (less than 200 m) or in transitional zones between upland

forest and alluvial plain of the Amazon River or its tributaries. This group of soils has

contrasting characteristics, with the upper part being very acid, with low base saturation

and high exchangeable aluminum. The same soil, at a depth between 2 to 3 m has a very

high base saturation, no exchangeable aluminum, and neutral or slightly alkaline pH. The

upper layer of these soils and the immediate subsoil are porous and water permeable,

whereas the deeper layer is water saturated due to a low permeability. Clay and other

textures are found in those soils.

The above description coincides in many aspects with the features of the lick and

their associated non-lick samples described in this study. It is possible, then, that the licks

in the Yavari-Miri valley are associated to a similar type of soils under comparable

erosion processes.

In the topsoil, when leaching removes Ca and other bases, pH reduces in

approximately the same proportion (Brady 1974). At lower pH, more Al is free in the

soil, reducing availability of other cations. Soil materials less exposed to leaching have

higher pH, and consequently less free aluminum. Kauffman et al. (1998) found that

critical pH after which there is no interchangeable Al in the soils of upland forest around

Iquitos is 5.5. This coincides with the absence of free Al in the lick samples, since all of









them had pH >5.5. As seen here, when pH is high, as in the lick samples, not only 1 but

several cations (such as Na Ca2+, Mg2 and K ) become more available.

The presence of carbonates in the licks also indicates that less altered parent

materials are the constituents of the licks of the middle course of the Yavari-Miri River.

For these reasons more than one element (bases) are available at the licks.

In general, nutrient availability in soils has been studied mainly in relation to plant

nutrition, but not in direct association with animal nutrition. However, consumption of

mineral-rich soil has been interpreted as a strategy to alleviate mineral deficiencies or

imbalances in the diet of some animals. Evidence supporting the hypothesis that soil

intake may help in reducing mineral deficiencies was summarized by Kreulen and Jager

(1984) and includes: (1) the ability of grazing livestock to choose supplemented salts

containing elements that are deficient in their diets, (2) in vivo and in vitro experiments

showing increase of macro and micronutrient levels in digestive liquors by elements

released from ingested soil, and (3) increase in absorption and retention of several

minerals by adding soil or clay to the diet of some domestic animals.

In southern Amazon, however, Gilardi et al. (1999) did not find significant

difference in the release of Na in an in vitro experiment by adding soil to an acid

environment, simulating the parrots gut conditions, and concluded that lick soils were not

a significant source of Na for the parrots, although Na content was higher in lick samples.

These researchers did not provide, however, information on the mineral content of the

parrots diet, making it difficult to see whether other minerals could be of importance for

the birds. Instead, they found support for the detoxification hypothesis, in part because of

higher clay content in lick samples. In contrast, the natural licks we studied in the Yavari-









Miri River valley did not show consistent differences in clay content, but they did

consistently show higher concentrations of several elements as compared to non-lick

soils.

It is possible that more than one type of lick exists in the Amazon, and that they

have different origins, and properties. The role of natural licks may vary across species as

suggested by other researchers in several parts of the world (Kreulen 1985; Diamond et

al. 1999; Klaus & Schmid 1998; Krishnamani & Mahaney 2000).

Since the licks studied in the Yavari-Miri River valley showed a higher

concentration of several elements, it is possible for animals to exploit them according to

their needs. Elements sought by animals will depend on the properties of their food, and

especially their elemental concentrations. In Chapter 4, element concentration in the food

of the lowland tapir, the most frequent lick user in the Yavari-Miri River, is examined.

Summary and Conclusions

The purpose of this chapter was to describe the natural licks occurring along the

middle course of the Yavari-Miri River, and to establish whether they were a source of

mineral nutrients and/or clay for herbivores. Another objective was to examine whether

licks maintain their mineral concentration through the year. Most licks were located on

sedimentary plains, and most seem to be related to the deposits of the Pebas formation.

Mineral content of licks was higher than non-lick samples, and did not drop through the

year. Some elements such as Na and Ca even increased in concentration during the drier

months, probably because leaching is reduced during those months.

Several elements were available and potentially used by the animals in the Yavari-

Miri River valley. Among macrominerals, Na, Ca, Mg and P had consistently higher

concentrations in licks than non-lick samples. This is related to the low alteration of the









sediments that form the licks. Also, among microminerals, Cu, S and B were more

concentrated in the licks. Overall, our results indicate that natural licks represent a source

of minerals for wildlife in the Yavari-Miri River valley. Whether animals use licks for

one or more minerals would depend on the mineral concentration of their food and their

potential needs for specific elements, which probably varies across species. Further

research is needed in order to examine the mineral concentration foods eaten by lick users

in the Amazon forest. A study in this direction was conducted for one of the most

frequent lick visitors, the lowland tapir (Chapter 4).

Table 3-1. Number of soil samples from lick and non-lick sites gathered in year 2001 in
the Yavari-Miri River valley in the Peruvian Amazon.

Lick number High water season Low water season
Lick soils1 Non-lick Lick soils1 Non-lick
soils2 soils2
1 2 1 2 1
2 2 1 2 1
11 2 1 2 1
12 1 1 1 1
13 2 1 2 1
15 2 1
16 2 1 3 1
18 2 1
19 2 1 1 1
20 1 1
21 2 1
22 1 1
24 1 1
Total samples 13 7 22 13
1 Number of licking sites inside each lick; a sample was taken from each site
2 Matched control samples taken within 10-20 m outside the licks
All samples (lick and non-lick soils) were composed of 3-4 sub-samples










Table 3-2. Descriptive features of 24 natural licks in the upper Yavari-Miri River valley,
Peruvian Amazon.
Location


Coordinates


Distance Elevation I


Lick
Number


1*
2*
3
4
5
6
7
8
9
10
11*
12 *
13*
14 *
15*
16*
17
18*
19*
20*
21*
22*
23
24*


Mean natural-lick size (sq meters + standard deviation)
Total area of natural licks (square meters)
* Licks sampled for soil analyses


SI Phnu


Lick type2 Size


from
Latitude Longitude river
(m)
-0422.16 -7211.57 1,300
-0422.10 -72010.28 1,350
-0422.70 -7211.91 564
-0421.90 -7212.47 1,326
-0422.54 -7211.91 533
-0427.43 -7219.50 733
-0427.30 -7219.62 1,050
-0427.69 -7219.21 100
-0426.58 -7219.54 1,685
-0426.80 -7220.95 3,500
-0426.17 -7218.60 770
-0430.47 -7225.26 625
-0430.73 -7225.26 310
-0420.08 -72010.93 586
-0423.70 -7215.19 500
-0423.11 -7215.24 1,500
-0430.80 -7225.74 0
-0429.79 -7225.72 1,800
-0429.78 -7225.78 2,000
-0425.51 -7218.39 880
-0424.50 -7219.01 3,030
-0423.56 -7219.52 5,400
-0430.62 -7225.23 590
-0430.67 -7225.25 380


(m2)


1,196
201
25
80
30
25
30
400
15
35
928
81
293
100
436
1,010
25
180
527
357
323
814
10
161


7,282


PhU = Physiographic Unit; SP = Sedimentary Plain; FP = Flood Plain.
2 Lick type: Upland = licks appear as depressions in upland forests, usually with large
stones and caves or mined holes; Low Bajial = licks are on areas flooded for several
months; High bajial = licks are on areas intermittently flooded for days to several weeks;
Riverbank = licks are on the cliffs of the Yavari-Miri riverbank, and are under water
several months a year.
3 GS = Number of geophagical spots (where animals actively consume soil) inside each
natural lick


Upland
Upland
Upland
Upland
Upland
Upland
Upland
Low bajial
Upland
Upland
Upland
Upland
High bajial
Low bajial
High bajial
Upland
Riverbank
Upland
Upland
Upland
Upland
Upland
Upland
High bajial
300 + 351














Table 3-3. Chemical characterization of soils from lick and non-lick sites in two seasons of year 2001 in the Yavari-Miri River valley
in the Peruvian Amazon.
High water season Low water season
Feature Lick Soils Non-lick Soils Paired t-test Lick Soils Non-lick Soils Paired t-test
(n = 13) (n = 7) p-value (n = 22) (n = 13) p-value
Mean SD Mean SD Mean SD Mean SD
pH (1:1 soil:water) 7.41 + 0.54 4.61 + 0.63 6.95 0.82 5.15 + 0.61
Organic Carbon (%) 1.26 + 1.03 0.84 0.26 1.22 + 0.88 0.60 + 0.27
Samples with CO3 (%)1 84.61 0 59.09 15.38
P available (ppm) 82.55 38.90 2.57 + 2.27 0.001 85.90 + 50.39 22.05 + 35.52 0.001
Al3+ (meq/100 gr) 0.00 11.65 6.85 0.027 0.128 12.88 7.48 0.009
CEC (meq/100 gr) 21.88 + 4.32 23.32 + 5.87 22.46 + 4.33 25.22 + 5.76
Base Saturation (%) 97.6 to >100 57.9 13 79.3 to > 100 47.00 21.1
Extractable bases
Ca2+ (ppm) 4114.00 + 941.00 1969 541.00 0.001 4385 1324 2031 + 1395 <0.001
Mg2+ (ppm) 720.00 326.00 375.00 202.00 0.001 764 355 338 + 168 <0.001
K (ppm) 75.49 + 32.57 65.91 + 29.47 0.520 99.88 30.80 86.92 + 31.53 0.333
Na+ (ppm) 67.82 + 44.90 6.87 + 4.39 0.014 102.74 + 57.92 17.79 + 9.94 <0.001
1 The value refers to the percentage of samples that had positive reaction to 10% HC1, indicating the presence of carbonates in the
sample.
* No test
SD = Standard deviation









Table 3-4. Microminerals in lick and non-lick soils during the high water season of 2001,
in the Yavari-Miri River valley in the Peruvian Amazon.
Element Lick Soils Non-lick Soils Paired t-test
(n = 13) (n = 7) p-value
Mean SD Mean + SD
B (ppm) 0.32 + 0.20 0.13 + 0.04 0.006
Cu (ppm) 3.08 1.12 1.12 0.83 0.012
Fe (pmm) 95.51 69.73 55.81 29.06 0.156
Mn (ppm) 19.33 + 15.31 51.53 +49.82 0.164
Zn (ppm) 2.17 + 0.99 1.39 +.090 0.282
S (ppm) 141.74 + 153.93 6.79 3.91 0.020










\.











a Natural licks 3000 0 3000 6000 Miles

Geomorphological units
Flood Plain
Sedimentary Plain
Terraces




Figure 3-1.Location of the study site in the Yavari-Miri River valley, in northern
Peruvian Amazon.






57




60 U Lick
50 E- Non-Lick


30
0 20
U 10


Sand Silt Clay
Particle Size

Figure 3-2.Mean content of sand, silt and clay in samples from lick and non-lick soils.
Size of vertical lines indicates + 1 standard deviation.














CHAPTER 4
BROWSE AND FRUIT AS A SOURCE OF MINERALS FOR LOWLAND TAPIR IN
THE YAVARI-MIRI REGION

Introduction

Lowland tapir (Tapirus terrestris) is the largest wild terrestrial mammal of the

South American tropics (Eisenberg 1989). Average adult weight varies from 150 to 300

kg, with females being slightly heavier than males (Padilla & Dowler 1994, Emmons &

Feerl997, Shoemaker et al. 2004). Tapirs are odd-hoofed ungulates, and are related in

their phylogeny to horses and rhinoceroses, sharing with them several morphological and

physiological characteristics. For example, like horses and rhinos, tapirs are non-

ruminants, and have a relatively simple stomach contrasting with a large cecum and a

voluminous and enlarged sacculated colon (Stevens 1988), and have hindgut

fermentation (Janis 1976). However, unlike horses and some species of rhinos, tapirs are

browsers/frugivores (Bodmer 1990), and live primarily in humid tropical forests.

In several sites of the Amazon forest, especially in western Amazonia, lowland

tapirs frequently visit natural licks (Pefia et al. 1996; Montenegro 1998), and may spend

on average half an hour in geophagy (ingestion of soil materials) (Montenegro 1998).

Lowland tapirs are the most frequent nocturnal species visiting natural licks in the

Yavari-Miri River region of the northern Peruvian Amazon (Chapter 2). This habit seems

to be related to the tapir's nutritional ecology. Analysis of consumed soils in the Yavari-

Miri region revealed a higher concentration of several elements (P, Ca, Mg, Na, B, Cu

and S) as compared to control samples outside the licks (Chapter 3).









One common hypothesis is that animals engaging in geophagy are under some kind

of stress, often of nutritional nature. Several studies have investigated the chemical

characteristics of the eaten soils to identify which elements are in higher concentration at

licks, in order to explain geophagy in some species (Emmons & Stark 1979; Jones &

Hanson 1985; Tracy & McNaughton 1995). However, often more than one element is in

higher concentration in consumed soils, making it difficult to associate soil consumption

to a particular mineral nutrient. Often, low levels of dietary sodium in tropical areas

explain geophagy in both wild and domestic animals such as elephants (Holdo et al.

2002) and cattle (McDowell 2003). In addition, several studies have found that in

temperate areas many ungulates also obtain Ca or Mg from licks (Jones and Hanson

1985). Also, some trace minerals such as Se and Co could be obtained from ingested soils

(Grace et al. 1996; Underwood and Suttle 1999).

The nutritional importance of soils as a dietary source of minerals depends on the

amount of soil ingested, the ratio of mineral concentration in soil to that of consumed

plants, and in the ability of the animal to extract and absorb elements directly from the

soil (McDowell 2003). For many wildlife species, however, information on the mineral

concentration of their foods is unknown, making it difficult to identify potential mineral

deficiencies or unbalances that could be driving animals to consume soil.

Although the lowland tapir's diet has been studied in several tropical locations such

as Peru (Bodmer 1990), Brazil (Fragoso 1997; Olmos 1997; Fragoso et al. 2000; Galetti

et al. 2001), Venezuela (Salas and Fuller 1996), French Guiana (Henry et al. 2000), and

Colombia (Pefia et al. 1996), very little is known about the nutritional contents of foods

eaten by tapirs in the wild, except for some reports of fat, carbohydrate and protein









content of several Amazonian fruits (Lopes et al. 1980). Also, mineral requirements and

status of tapirs in the wild are unknown, making it difficult to identify any deficiency or

unbalance that may be driving them to visit natural licks.

In captivity, tapirs are usually fed following guidelines for horses, due to their

similarity in digestive system anatomy (Barongi 1992; Janssen et al. 1999; Shoemaker et

al. 2004). Those diets comprise legume hay, herbivore pellets and commercial produce

and/or harvested browse plants, and mineral supplementation when needed (Shoemaker

et al. 2004). In the wild, however, lowland tapirs feed on a large amount of fruits,

relatively high for a herbivore of that size (Bodmer 1990). They also consume leaves and

fiber (other plant parts such as stems, bark or wood) (Bodmer 1990; Henry et al. 2000).

Although estimation of percentages of each of these 3 items may vary according to food

available, studies in the Amazon and French Guiana have shown that at least 30% of the

lowland tapir's diet is comprised of fruit, and the remainder made up of varying amounts

of leaves and fiber (Bodmer 1990; Henry et al. 2000). In French Guiana, lowland tapirs

may consume up to 70% of fiber (Henry et al. 2000).

It is unknown, however, whether lowland tapirs can obtain all their necessary

nutrients exclusively from food. Since lowland tapirs frequently visit natural licks that are

rich in several minerals in the Yavari-Miri River valley, lowland tapir food in this area

might be limited in some elements. Since no seasonality was found in lick use in the

Yavari-Miri region (Chapter 1), any potential nutritional limitation in tapir food related to

lick use is expected to be present all year around.

An indirect way to examine potential deficiency of one or more minerals is by

examining fecal excretion of such minerals. Fecal mineral content has been used in other









herbivores as a method to examine mineral status, particularly for sodium (Khalili et al.

1992; Studier et al. 1994), or absorption, particularly for calcium (Schryver et al. 1983).

In cases of depletion, fecal excretion of some minerals (i.e. sodium and phosphorus

among others) reduces considerably, in some cases virtually to zero (i.e. phosphorus)

(McDowell 2003).

If tapir food is limited in one or more mineral nutrients throughout the year, very

little excretion of such minerals (at least for sodium and phosphorus) is expected in feces,

unless such limitation is alleviated by other sources. If tapirs consume mineral rich soils,

naturals licks, may represent a critical resource for lowland tapir nutrition, and overall,

their persistence in western Amazonia.

The purpose of this chapter is to evaluate lowland tapir's food as a source of

minerals in the Yavari-Miri River valley. The main hypotheses examined in this chapter

are the following:

* Hypothesis 1. Lowland tapir food is limited in one or more mineral nutrients in the
Yavari-Miri River valley, and such limitation is constant through the year.

* Hypothesis 2. Excretion of limited minerals (at least for some minerals) is low in
tapir feces.

To test these hypotheses, the diet of lowland tapir in the Yavari-Miri River was

studied, and the mineral content of the most frequently eaten foods was analyzed. Also,

analyses of minerals in lowland tapir feces were conducted to examine fecal mineral

excretion. If lowland tapirs eat mineral rich soils at natural licks because of a mineral

nutritional deficiency or unbalance, it is expected that: (1) one or more elements in tapir

food are low in comparison to mineral requirements of lowland tapirs, (2) no significant

changes occur in the mineral content of tapir food through the year, and (3) mineral









concentration of one or more minerals in tapir feces would be higher than expected if the

animals are facing a deficiency of such minerals.

Study Area

This study was conducted in the middle course of the Yavari-Miri River, in the

Peruvian Amazon, in the area between 4o30.23'S, 7226.69W and 4o24.77'S,

7209.76'W. Weather in the area is characterized by a mean annual temperature of 26C,

with mean maximum temperatures ranging from 28-30C, and mean minimum from 17-

20C (Marengo 1984). Mean annual precipitation varies from 2400 to 3100 mm, with the

highest monthly rainfall occurring from February to April, and the lowest from June to

September. The water levels are the lowest during the months of less rainfall (June to

September), and the highest during the months of maximum precipitation (February to

May).

Plant diversity in the area is very high. Recent estimates indicate that number of

plant species in the Yavari region may reach up to 3,500 species (Pitman et al. 2003).

Habitat types in the area include upland and flooded forests. Upland forests are very

diverse and vary greatly with soil characteristics (Roukolainen & Tuomisto 1993).

Flooded forests tend to be heterogeneous and continually changing due to the river

fluctuations (Puhakka & Kalliola 1993). Among flooded forests, swamp forest, is

common along these rivers, covering 25-50% of the flood plains (Pitman et al. 2003).

Methods

Lowland Tapir Diet in the Yavari-Miri Region

Diet of lowland tapir in the Yavari-Miri region was studied through both

examination of feeding signs and inspection of tapir feces. A search for tapir feeding

signs was conducted along 26 trails opened on both sides of the Yavari-Miri River, from









January to December 2001. Trail length varied from 2 to 5 km, for a total of 65.8 km of

trails. Once a feeding sign was found, browse clearly eaten by tapirs was collected. When

feeding on leaves, tapirs usually pull down branches and stems, leaving teeth marks on

the bark (Salas & Fuller 1996), and very often may cut the stem at about 1 m from the

ground (usually when it is up to 2 cm in diameter), leaving a characteristic feeding sign

of a broken stem with its upper part hanging down. When feeding on lower vegetation,

especially from plants growing in gaps, tapirs eat leaves from young plants up to 1.5 m

above ground (personal observation), and the feeding sign is unmistakable. In addition,

since tapirs also feed on fruits (Bodmer 1990; Olmos 1997; Henry et al. 2000), several

fruits were collected from tapir feeding sites. In all cases, tapir feeding was confirmed by

the presence of tapir tracks at the feeding site, and only browse or fruits undoubtedly

eaten by lowland tapirs were collected.

Composite samples from every browsed plant were collected with stainless steel

scissors and rubber gloves, and placed in cotton bags. Samples were air-dried for several

days and stored in dry plastic bags until they were analyzed for mineral content. Also, a

part of the fresh sample was prepared as botanical vouchers for species identification.

Voucher samples were sun dried for several days and stored. Fruit samples were

preserved in 95% ethanol in tight plastic containers until they were dried for mineral

analyses later. Fruit samples were dried in an oven at 60C for 24 hours prior to mineral

analysis. Botanical vouchers were identified at the Herbarium Amazonense (AMZ) in

Iquitos, Peru. Voucher specimens were deposited at the same herbarium. Plant

identification follows nomenclature from Gentry (1996).









Also, lowland tapir feces were collected along trails, from streams, and to a lesser

extent, from tapir latrines. Fecal samples were sun dried for several days and stored for

further analyses. All samples were handled with rubber gloves and placed in individual

clean plastic bags. About 50 % the feces samples was examined for proportion and

frequency of occurrence of food types (fruits, leaves and fiber), following Bodmer

(1990), with the difference that no stomach samples were used in this study. The

remaining 50% of the samples, mainly the most fresh, were left for examination of

mineral content.

Determination of Minerals in Tapir Food and Fecal Samples

Browse, fruit and fecal samples were analyzed for concentration of nitrogen and 11

minerals: 6 macrominerals (P, K, Ca, Mg, S and Na) and 5 trace minerals (Mn, Zn, Cu,

Fe, and B). Laboratory analyses were conducted in the laboratory of soils, water and

plant tissues of the Institute for Agriculture (CORPOICA) in Colombia. Samples were

pretreated (or mineralized) with a wet oxidation-digestion procedure to remove organic

matter. Reagents for this procedure were Nitric and Perchloric acids in proportion 3:2.

Digestion was conducted by gradually increase of temperature at 100C intervals up to

300-330C approximately, in a Tercator digester. Part of the resulting aqueous solution

was completed with water and concentration of Fe, Cu, Mn, and Zn was determined in an

atomic absorption spectrophotometer Perkin Elmer 2380. For determination of K, Ca, Mg

and Na, lanthanum was added to another part of the aqueous solution and their

concentration was determined also by atomic absorption spectrophotometry. Phosphorus

concentration was determined by adding a colorimetric reagent of ammonium and

potassium tartrate, sulfuric acid, ammonium molybdate, and ascorbic acid to the aqueous

solution containing the minerals, reading the absorbance of the solution in a Milton-Roy









light spectrophotometer, and comparing with a calibration curve. Sulfur concentration

was determined also by spectrophotometry, after adding a solution of nitric and acetic

acids and a turbidimetric reagent of bactogel and barium chloride to the aqueous solution

containing the minerals.

To determine Boron and Nitrogen content, non-digested samples were used. For B,

1 g of plant tissue was mixed with 0.1 g of calcium oxide and dry ashed in a muffle

furnace at 500C. Ashes were mixed with sulfuric acid, filtered and mixed with Azometin

H for color development, and concentration of B was determined by spectrophotometry.

Nitrogen was determined with the Kjeldahl method (Ma & Zuazaga 1942).

Data Analyses

Assumptions of normal distribution and homogeneity of variances were tested for

all variables with the Kolmogorov-Smirnov test and Lavene's test respectively. When

assumption of normality was not met, alternative non-parametric tests were used. For

testing differences between 2 groups, t-tests or the Wilcoxon test were used. When

comparing more than 2 groups, a one-way Analysis of Variance (ANOVA) or

alternatively the Kruskal-Wallis test were used. If differences were found when

comparing more than 2 groups, further multiple comparisons were done with the Tukey

test to find which groups were different. For all tests, a p <0.05 was considered

significant. Mean concentration of each mineral in leaves was compared between high

water and low water seasons. Also, mineral content of leaves was compared among the

most common plant families in tapir's diet. Mean concentration of each mineral was

compared between leaves and fruits. Finally, mean concentration of each mineral in feces

was compared to mean concentrations in both leaves and fruits separately. All statistical

analyses were performed with the software SPSS version 11.5 for Windows.









Results

Lowland Tapir Diet at the Yavari-Miri Region

A total of 134 browse samples was collected from the forest on both sides of the

Yavari-Miri River. Samples represent 31 plant families, 63 genera and 89 species (Table

4-1). The most common lowland tapir's browse was from the Melastomataceae (22%)

and Rubiaceaae (17%) families (Figure 4-1). The next most common families in tapir

browse were Areaceae (6%), Myristicaceae (5%), Fabaceae (4.47%), and Sapotaceae

(3.73%). The remaining species represented from <1% to 2.2 % of tapir's browse (Figure

4-1).

A total of 72 tapir fecal samples was collected from January to December 2001.

80% of those samples were found in shallow water, along banks of small streams, while

only 20% were found on the ground, in tapir latrines. Tapir latrines were found only

twice in this study. A total of 37 fecal samples were sent to the laboratory for mineral

analyses. The remaining 35 samples were examined for determination of the components

of tapir's diet. Fruit parts, leaves, fibers (stems, wood, and other fibrous plant materials),

and soil were found in tapir feces. Percentage of occurrence of these items in feces was

96.6% for fruit parts, 100% for leaves and fibrous materials, and 76.6% for soil.

Proportions of these items on a dry matter basis were the following: fruit parts 8.89 +

9.33% (range 0 43.75%), leaves 75.42 16.91% (range 18.09 90.22%), fibers 12.54 +

13.27 % (range 2.17 68.09%) and soil 3.20 3.14% (range 0 8.42%). The proportion

(on a dry weight basis) of fruit in tapir diet is underrepresented. All but one fecal sample

analyzed for diet components had fruit remains (exocarps and seeds), but their weight

was comparatively low because the largest seeds are spit out and are not in the feces,









although the pulp was consumed in large amounts. This was observed in other studies

where stomach contents were analyzed (Bodmer 1990; Henry et al. 2000). In

consequence, real proportion of fruit in tapir diet in the Yavari-Miri River is higher than

the average shown above.

Tapirs ate at least 14 fruit species (Table 4-3). The most common fruits found in

tapir feces and their percentages of occurrence were the following: Mauritiaflexuosa

(70%), Annona spp (40%) Spondias mombin (40%), Oenocarpus bataua (35%), Couma

macrocarpa (25%), and Attalea sp. (15%) (Figure 4-2). Also, from feeding signs along

tapir trails, we found that fruits of a species of Moraceae (Ficus insipida) are also part of

the tapir's diet (Table 4-3).

Minerals in Lowland Tapir Food

Concentration of minerals in lowland tapir's browse was analyzed in 37 leaf

samples, representing 32 species (Table 4-1). Analyzed samples included the most

common species browsed by lowland tapirs. Mean concentrations of macrominerals (P,

K, Na, Mg, S and Na) and trace elements (Mn, Zn, Cu, Fe and B) in tapir browse are

illustrated in Figures 4-3 and 4-4, respectively. No seasonal differences were found in

macromineral concentration in tapir browse (p>0.05 in all tests), except for a barely

significant difference in P during the low water season (t =2.05, df=35, p =0.047) and a

higher concentration of Mg during the high water season (t = 2.2, df = 35, p = 0.034).

Although K seems to be at higher concentrations in the low water season, there was large

variation among samples, and the statistical test was not significant (Wilcoxon's test z =

0.68, p = 0.50). Among trace elements, only Fe (t = 2.3, df= 35, p =0.008) was different,

occurring at higher concentration in browse collected during the low water season (Figure

4-4). Although mean concentration of Mn looks higher also during the low water season,









large variation within samples yielded a non-significant test (Wilcoxon't test z = 1.4, p=

0.14).

Since tapirs eat leaves mainly from the Melastomaceae and Rubiaceae families,

mean concentrations of minerals were compared among those families, pooling the other

families as a third group. Differences were found only for Ca (F2,34= 5.3, p = 0.010) and

Mg (F 2,34 = 4.1, p = 0.024). Higher concentration of Ca was found in leaves of the

Melastomaceae and Rubiaceae family, whereas Mg was more concentrated in leaves of

the Rubiaceace and the other group of families.

Although 14 samples of fruits were collected, the amount of dry pulp was enough

for analyzing only 4 fruit species (Mauritiaflexousa, Spondias mombin, Couma

macrocarpa and Jacarantia sp.). These species, however, were among the most frequent

in tapir diet (Figure 4-2), and may give a good idea of the quality of fruits as a source of

minerals in tapir's food. When compared with browse, differences were found for 2

macrominerals (K and Na) and 2 trace elements (Mn and Fe). All these 4 elements were

at higher concentrations in browse than in fruits (Wilcoxon's test: z = 3.07, p = 0.002 for

K, z = 3.26, p = 0.001 for Na; z = 2.98, p = 0.003 for Mn, and t = 4.8, df = 22.9, p <0.001

for Fe). Mean concentration of Na was particularly low in fruits (0.03%+0.01).

Since tapir mineral requirements are unknown, concentration of minerals in tapir

food was examined in relation to minimal requirements for horses (NRC 1989) because

of their similarity in digestive system (Janssen et al. 1999). Levels of P were below

minimal required concentrations in horse diets (Table 4-4) in both browse and fruit

samples. P levels were much below the minimal requirement for growing horses or

pregnant females (Table 4-4). Although mean P level in browse was slightly higher in the









low water season, its concentration was lower than required in both seasons. Mean Na

concentration in browse samples was within the minimal required for horses, but below

requirements in all fruit samples (Table 4-4). Potassium levels were below requirements

only in fruit samples. The remaining macrominerals were within the minimal required

levels for horses, in both browse and fruit samples.

Among trace elements, Zn concentration was below minimum requirements for

horses in both browse and fruits, and Cu was below requirements in browse and barely at

a minimum requirement in fruits (Table 4-5). However, Cu requirements for tapirs may

be much higher than the requirement for horses (Janssen et al. 1999), suggesting that both

browse and fruits would be deficient in Cu in tapir diet. In contrast, levels of Mg and Fe

were much higher than required in horse diets (Table 4-5). Concentration of B was

similar between browse and fruit samples, but requirements have not been established in

horse diets. Besides minerals, both browse and fruit samples showed high levels of crude

protein (measured as N concentrations) (Table 4-5). In summary, minerals in tapir diet in

the Yavari-Miri River seem adequate except for P, Na, Zn and Cu, based on requirements

established for horses.

Mean fecal concentration of minerals is shown in Table 4-5. Among

macrominerals, levels of P in feces were similar to those in browse and fruit.

Concentration of Na in fecal samples was higher than the one in browse and especially

fruits. Fecal concentrations of other macrominerals were always lower than

concentrations in tapir foods. Most trace elements where at higher concentrations in fecal

samples than in tapir foods especially for Fe, Zn and Cu. Fecal Fe was particularly high









in fecal samples. The only exception was Mn, which was lower in feces than in browse,

but was higher than in fruit samples. No fecal B was analyzed.

Discussion

Lowland Tapir Diet at the Yavari-Miri Region

Lowland tapir diet at the Yavari-Miri River is composed of a large number of plant

species. This result agrees with previous research in other tropical forests. For example,

in the Tabaro River valley of Venezuela lowland tapirs also feed on 88 plant species

(Salas 1996), and on 81 species in the Duda River of Colombia (Pefia et al. 1996).

Most browse samples were found in tree fall gaps or early successional stages of

riverbank vegetation were plants from the Melastomataceae and Rubiaceae were

growing. Those two families are typical of second growth states and are usually

represented by pioneer species. Salas and Fuller (1996) also found such foraging

behavior of lowland tapir in the Tabaro River valley (Venezuela), and established that

tapirs are more selective when foraging in sites other than tree fall gaps. In the Yavari-

Miri River valley tapirs foraged also on growing trees with trunks > 2 cm in diameter or

semi-epiphyte plants (family Araceae) growing on tree trunks. Tapirs ate those plants

mainly during their young states. Frequency of browsing on fast growing plants seems to

be a characteristic of tapirs in general, according to the list of browsed species reported in

the diets of the other 3 tapir species (Janzen 1982a;Terwilliger 1978; Naranjo 1995;

Foerster 1998; and Tobler 2002 for Tapirus bairdii; Downer 2001 for Tapiruspinchaque;

and Williams 1980 for Tapirus indicus).

Besides browse, fruits are very important in the tapir's diet. This feature was also

described in the Blanco River of Peru (Bodmer 1990), French Guiana (Henry et al.

2000), Colombia (Pefia et al. 1996) and Brazil (Fragoso 1997; Fragoso & Huffman









2000). The most common fruits eaten by lowland tapirs in the Yavari-Miri River were

from Mauritia palm (Mauritia flexuosa) and trees of Spondias mombin, Couma

macrocarpa and Oenocarpus bataua, among others. Tapirs consume the same fruit

species in other tropical forests and disperse many of their seeds (Olmos 1997; Fragoso

1997; Fragoso et al. 2003). Overall, fruits consumed by lowland tapir in the Yavari-Miri

River are very similar to those described for the Blanco River (Bodmer 1990), located

about 100 km northwest of the Yavari-Miri river, in the same continuous forest. The

highest percentage of occurrence of the palm Mauritiaflexousa and the occurrences of

other fruit species is common in both areas. This resemblance is expected, since it is the

same forest, and overall plant composition in both areas is probably very similar.

Proportion (on a dry basis) of fruit in tapir diet in the Yavari-Miri River estimated

from fecal examination seems lower than in the Blanco River, but this result does not

really reflect the real proportion of fruits in the diet, since the largest seeds are not in

feces. As noted by Bodmer (1990) and Henry et al. (2000) tapirs spat out the seeds of

Mauritiaflexuosa, but large amounts of its pulp were in stomach samples. These fruits

are large (about 50-60 cm long and 30-40 cm in diameter) and are covered by very small

scales. Seventy percent of fecal samples from the Yavari-Miri valley had large amounts

of Mauritiaflexuosa scales. Bodmer (1990) found a similar percentage of occurrences for

Mauritiaflexuosa (76.3%), examining both fecal and stomach samples. For this reason, a

proportion of 33% of fruit in tapir diet (obtained from both stomach and fecal

examination) in the Blanco River (Bodmer 1990) is probably a better estimation on the

true proportion of fruit in the diet of tapirs at the Yavari-Miri River. Other plant parts,

such as stems, bark or wood (termed fiber in several studies) was found in tapir feces in









variable amounts from about 2-68% on a dry matter basis. This result indicates that tapirs

feed not only on leaves and fruits. Fibrous materials may represent a significant portion

of tapir feeding habits in some circumstances. For example, fiber content in tapir diet was

very high during the low fruit production season in French Guiana (Henry et al. 2000).

Soil also was found in 76.6% of the tapir feces analyzed, indicating that tapirs often

consume soil. Since tapirs purposely visit natural licks (Chapter 2), soil consumption is

not accidental. The amount of soil in feces was however relatively low (3.2% of fecal

sample on a dry matter basis), indicating that tapirs eat soil frequently, but in relatively

small amounts. Soils are never discussed as part of tapir diet since this behavior has been

either disregarded or considered abnormal. In fact, soil consumption is often seen as a

type of pica, a behavior that refers to consumption of abnormal materials with no

nutritional value (Maynard et al. 1979). Overall, tapir diet in the Yavari-Miri River is

composed of a large diversity of browse, mainly from growing plants, a significant

amount of fruits, mainly palm fruits, and variable amounts of fiber.

Minerals in Lowland Tapir Food

Animals derive the majority of their mineral needs from their food. For herbivores,

however, sources of some minerals may be limited, depending on the characteristics of

the soil and vegetation. Poor mineral content in vegetation may result in nutritional

deficiencies if animals do not find alternative mineral sources.

Most minerals in lowland tapir diets seem adequate in browse and fruits based on

suggested requirements for horses, except for Na, P, Cu and Zn. Although mean Na in

browse did not appear too low, about 50% of individual samples had Na concentration

below the average. Also, Na intake from tapir food is probably low, considering that

browse accounts for only a portion of tapir food. Fruits had very low Na concentrations,









and they comprise a significant part of tapir diet. Unfortunately tapir mineral

requirements have not been assessed, and the assumption that their requirements are the

same as horses may be inadequate for some minerals. Horses are primarily grazers

feeding on high fiber diets. The digestive system of tapirs is less specialized than that of

horses for fiber digestion (Janis 1976). Data from captive animals suggest that

comparative digestibility of cellulose and hemicellulose is slightly lower in tapirs than in

horses (Janssen et al. 1999). Tapir fecal samples often contain entire leaf fragments and

large fibrous materials. Coarsely chewed forages also were observed in fecal samples

from the Malayan tapir in the wild (Williams 1980). These observations are in agreement

with a rapid rate of food passage in tapir digestive system. Efficiency of cellulose

digestion reduces with an increase in rate of passage. Rate of passage in horses is lower

than that of ruminants of similar weight (48 h vs 80 h) and efficiency of cellulose

digestion is 70% of that of a ruminant (Janis 1976). Na requirement in horses is higher

than the requirement for ruminants (0.10% vs 0.08% respectively). Although rate of

passage should not be a factor for Na, since this element is rapidly and almost completely

absorbed (McDowell 2003), the ability of tapirs to absorb Na in the lower part of the

gastrointestinal track is unknown. If digesta remains longer in the digestive tract, it is

possible that more cellulose will be broken down by microflora and thus release minerals

from lignin complexes. However, this is not expected in tapirs, since their rate of passage

seems to be very rapid.

Optimal Na concentration in equine diets has been suggested to be 0.16 to 0.18% of

dry matter for growth, maintenance and late gestation (Jarrige & Martin-Rooset 1981;

NRC 1989). Na concentration in 51% of browse samples and 100% of fruit samples was









below the above requirements, and tapirs could develop a Na deficiency, especially when

feeding mainly on fruits, if no other source of Na is available. Bioavailability of Na in

feeds is seldom addressed because normally sodium is added to the diet as salt

supplements (Ammerman et al. 1995) and it is almost completely absorbed.

Bioavailability of Na in tapir food is unknown and should be studied. In general, most

plant products have relatively small amounts of Na in comparison to animal products

(McDowell 2003).

Sodium (in addition to chlorine and potassium) is very important for maintaining

osmotic pressure and regulating acid-base equilibrium in organisms, functioning as an

electrolyte in body fluids (McDowell 2003). These elements are involved in cellular

water metabolism, nutrient intake and transmission of nerve impulses (McDowell 2003).

Sodium deficiency has been found in many tropical locations and is one of the factors

limiting animal production in some tropical countries (McDowell 1985). Tropical areas

with high rainfall are usually Na-depleted since this mineral is easily leached form the

soil and plants usually do not accumulate it -except for halophytes- (Robbins 1993).

Sodium is excreted mainly in urine and with smaller amounts in feces. When Na

intake is low the organism conserve this element by reducing its excretion (McDowell

2003). Based on the low Na concentration in tapir food (especially in fruits) below its

requirement, a potential deficiency could occur. In a deficiency status, tapirs should

reduce fecal excretion of endogenous Na, and very little amounts of this element would

be expected in tapir feces. However, fecal excretion of Na was not as low as expected if

tapirs were facing a deficiency of this mineral. Tapirs consume soils at natural licks and

those soils had higher concentration of Na as compared to non-lick soils. These results









agree with the hypothesis that tapirs obtain Na from natural licks. The same could be

suggested for other lick users. For example periodic Na deficiencies were suggested for

frugivorous bats in a location close to the Amazon and Napo Rivers (Studier et al. 1994),

a forest relatively close to the Yavari-Miri River forest. Such a deficiency results from

low Na concentrations of fruits. Frugivorous bats were very common lick users (Chapter

2).

The other macromineral that was low in tapir diet was phosphorus. Phosphorus and

calcium are major mineral constituents of the animal body (Robbins 1993). In bones the

ratio of Ca:P is usually constant and somewhat greater that 2:1 (McDowell 2003).

Phosphorus is fundamental in almost all aspects of animal metabolism, including energy

metabolism, muscle contraction, nerve tissue metabolism, transport of metabolites,

nucleic acid structure, and nutrient metabolism (Robbins 1993). Phosphorus absorption

efficiency in horses is 35%, but it may vary according to the form (organic or inorganic)

in diet, being reduced in diets with high concentrations of oxalates (NRC 1989).

Requirements in horses during gestation and lactation increase because of milk

production. Calcium was at adequate levels in tapir foods, but P was significantly low.

Ratios of calcium to phosphorus should be 2:1, but very low phosphorus intake is

detrimental (NRC 1989). Deficiency of P produces rachitic changes in growing horses

and osteomalacic changes in adult horses. In herbivores, P is excreted primarily in feces,

although animals fed high concentrated diets excrete P also in urine (McDowell 2003).

Levels of P in tapir feces were expected to be low since P in food was below

requirements for maintenance and very low for growth and lactation. As with Na, tapirs









may be adding P to their diets by consuming soils. Phosphorus was very high in licks

soils as compared to non-lick samples.

Among microminerals, Cu appears to be limiting in tapir diet. A potential

deficiency of Cu could be expected from tapir diet because tapirs may have a unique

metabolic requirement for this element (Janssen et al. 1999). This suggestion comes from

the observation that levels of Cu in 22 captive tapirs of 3 species had a mean serum

copper level of 0.21 [tg/ml when a normal level in horses is 0.7 ppm. Dietary copper

concentrations in those tapirs were adequate in comparison to horse requirements

(Janssen et al. 1999). Concentration of Cu in plants depends on several factors such as

form of soil copper, pH, concentration of other elements and organic residues and plant

species. Usually, severely leached, sandy soils, alkaline soils or peat or muck soils

produce plants with a low copper content. Absorption of copper tends to be low, and is

affected by chemical form, copper status of the animal and levels of other ions such as

calcium, cadmium, zinc, iron, lead, silver, molybdenum, and sulfur (Robbins 1993). A

high proportion of ingested Cu is excreted in feces, and most fecal Cu is unabsorbed

(McDowell 2003). Copper was also higher in lick soils as compared to non-lick soils

(Chapter 3). By consuming those soils, tapirs could be adding Cu to their diets.

Summary and Conclusions

Lowland tapir's diet in the Yavari-Miri River valley is very diverse, including more

than 80 species of browsed plants and at least 13 species of fruits. Most browsed species

are of the families Melastomataceae and Rubiaceae, and are pioneer plants growing in

tree fall gaps. Fruits eaten by tapirs represent several palms and other tree species. Diet of









lowland tapir in the Yavari-Miri River valley is similar to what is described for other

tropical locations.

Mineral contents in browse and fruits eaten by lowland tapirs seem adequate, based

on horse diets, except for Na, P, Cu and Zn, whose levels are below suggested

requirements, especially for growing and lactating female horses. Levels of Na, P and Cu

excreted in tapir feces are higher than expected if tapirs were facing a deficiency of these

minerals. These elements were found in higher concentrations in soils eaten by tapirs,

suggesting that geophagy at natural licks functions as natural supplementation of those

minerals in the forest.

These results suggest that tapirs, and possibly other lick users, obtain minerals that

are in short supply in their diets by consuming soils from natural licks. As a consequence,

natural licks may be a very important resource for lowland tapirs and possibly other

herbivore/frugivore species in the Yavari-Miri River.







78


Table 4-1. Plant species in tapir browse along the Yavari-Miri River, Peruvian Amazon.


Family
Anacardiaceae
Annonaceae
Apocynaceae

Apocynaceae

Araceae

Araceae
Araceae

Araceae

Araliaceae

Bignoniaceae

Blechnaceae

Bombacaceae
Capparidaceae

Clusiaceae
Clusiaceae
Clusiaceae

Combretaceae

Combretaceae

Combretaceae
Convolvulaceae
Cyclanthaceae
Ebenaceae

Ebenaceae
Euphorbiaceae

Euphorbiaceae

Euphorbiaceae

Euphorbiaceae
Fabaceae


Fabaceae


Species
Spondias mombin *
Oxandra euneura
Tabernaemontana
flavicans
Tabernaemontana
siphilitica
Anthurium
brevipedunculatum *
Heteropsis sp.
Philodendron
elaphoglossoides
Philodendron
rudgeanum
Dendropanax
arboreus *
Arrabidaea
bilabiata *
Salpichlaena
hookeriana
Matisia bracteolosa
Capparis
macrophylla
C /h i ',I h/itou sp. *
Garcinia acuminata *

Moronobea coccinea
Combretum
fruticosum *
Combretum
laurifolium
Combretum laxum
Maripa sp.
Evodianthus funifer
Diospyros
poeppigiana
Diospyros subrotata

Acalipha sp.
Conceveiba
rhytidocarpa
Didymocistus
chrysadenius *
Mabea elata


Inga alba
Inca capitata


F Family
1 Melastomataceae
1 Melastomataceae
Melastomataceae
1
Melastomataceae
1
Melastomataceae
2
1 Melastomataceae
Melastomataceae
3
Melastomataceae


Meliaceae

Moraceae

Moraceae


Moraceae
Myristicaceae

Myristicaceae
Myristicaceae
Myrtaceae

Myrtaceae

Myrtaceae

Nyctaginaceae
Nyctaginaceae
Ochnaceae
Ochnaceae

Olacaceae
Rhamnaceae


Rubiaceae

Rubiaceae

Rubiaceae
Rubiaceae

Rubiaceae


Species
Miconia nervosa *
Miconia splendens

Miconia ternatifolia *

Tococa capitata

Tococa caudata *
Tococa coronata

Tococa guianensis

Tococa setifera *

Trichilia pallida

Cecropia sp.

Naucleopsis sp. *
Sorocea hirtella

Otoba glycycarpa
Otoba parvifolia
Virola elongata *
Eugenia
myrobalana *

Myrcia paivae *

Myrciaria sp. *
Neea floribunda *
Neea spruceana *
Ouratea aromatica

Ouratea sp.
Heisteria cauliflora

amazonicus

Coussarea brevicaulis

Faramea multiflora
Psychotria capitata
Psychotria
cartagenensis
Psvchotria cincta *










Table 4-1 (continued)


Family
Fabaceae
Fabaceae

Fabaceae

Fabaceae

Flacourtiaceae

Flacourtiaceae

Flacourtiaceae

Hippocrataceae
Icacinaceae
Lecythidaceae

Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae
Melastomataceae


Miconia eriocalyx
Melastomataceae Miconia mazanana *


F Family
1 Rubiaceae
Rubiaceae
1
Rubiaceae
1
Rubiaceae
1
Rubiaceae


Species
Inga dumosa *
Inga
semialata
Machaerium
floribundum *
Macrolobium


Hasseltia floribunda

Ryania speciosa *
Tetrathylacium
macrophyllum
Salacia sp. *
Humirianthera ampla
Eschweilera
tessmannii
Coussarea brevicaulis
Henriettea lasiostylis *
Loreya mespiloides
Miconia amazonica


Sapotaceae
Sapotaceae
Solanaceae

Solanaceae
Solanaceae
Violaceae
Vochysiaceae
Vochysiaceae


Species
Psychotria deflexa
Psychotria
iodotricha *

Psychotria loretensis

Psychotria lupulina
Psychotria
poeppigiana *
Psychotria
tenicaulis *
Warszewiczia
coccinea
Micropholis egensis
Pouteria guianensis *

Cestrum microcalyx
Cestrum sp.
Solanum sp.
Leonia glycycarpa
Vochysia lanceolata
Vochysia
lomatophylla *
Non-identified *


F = Frequency of each plant species in tapir browse samples.
* = Samples analyzed for N and mineral (P, K, Ca, Mg, S, Na, Mn, Zn, Cu, Fe, B)
content.


Rubiaceae

Rubiaceae






80


Table 4-2. Number of composite samples of each family analyzed for mineral
concentrations in 2 seasons in the Yavari-Miri River valley, Peruvian
Amazon.
Season
Family
High water Low water

Araceae 0 1
Araliaceae 0 1
Bignoniaceae 0 1
Clusiaceae 0 2
Combretaceae 0 1
Euphorbiaceae 0 1
Fabaceae 0 2
Flacourticeae 1 0
Hippocrataceae 1 0
Melastomataceae 1 8
Moraceae 1 0
Myristicaceae 1 1
Myrtacea 3 0
Nyctaginaceae 0 2
Myrtaceae 0 0
Rubiaceae 2 3
Sapotaceae 0 2
Vochysiaceae 0 1
Non-identified 1 0


Total samples






81


Table 4-3. Fruits in lowland tapir diet in the Yavari-Miri River valley, northeastern
Peruvian Amazon.


Local name


Evidence
Feces Feeding
sign


Anacardiaceae
Annonaceae

Apocynaceae
Arecaceae
Arecaceae
Arecaceae
Caricaceae
Cecropiaceae
Celastraceae
Chrysobalanaceae
Fabaceae
Moraceae
Sapotaceae


Spondias mombin *
Annona sp.
Couma macrocarpa
*
Mauritia flexuosa *
Oenocarpus bataua
Attalea sp.
Jacarantia sp. *
Pourouma sp.
Maytenus sp.
Licania sp.
Hymenaea sp.
Ficus insipida
Pouteria sp.


Uvos
Sacha anona

Leche caspi
Aguaje
Hungurahui

Papaiya
Sacha uvilla
Sacha shushuhuashi
Parinari de altura
Azucar huayo
Oje
Sacha caimito


* Fruits analyzed for N and mineral (P, K, Ca, Mg, S, Na, Mn, Zn, Cu, Fe, B) content.


Family


Species









Table 4.4. Mean content of nitrogen and macrominerals in tapir foods (browse and
fruits), suggested requirements (based on guidelines for horses) and mean
concentrations of excreted N and macrominerals in tapir feces.


K Ca Mg


S Na


% dry matter


Tapir food


Mean
SD


3.44
1.13


0.12
0.05


Mean 1.20 0.11
SD 0.80 0.08


0.73
1.26

0.14
0.03


0.53
0.32


0.27
0.14


0.15
0.03


0.22
0.13


0.70 0.14 0.36 0.03
0.94 0.13 0.34 0.01


Required1
Maintenance
Growth
Females2


Tapir feces


0.17
0.17-0.38
0.34


Mean 2.38
SD 0.65


0.14
0.09


0.30
0.30
0.38



0.18
0.18


0.24
0.31 -0.68
0.45


0.09
0.10
0.10


0.15
0.15
0.15


0.10
0.10
0.10


0.26 0.12 0.09 0.29
0.21 0.7 0.05 0.25


SD = 1 Standard deviation.
1 Suggested requirements based on guidelines for horses (NRC 1989).
2 Suggested requirements for pregnant and lactating females based on guidelines for
horses (NRC 1989).


N P


Browse


Fruits









Table 4-5. Mean content of microminerals in tapir foods (browse and fruits), suggested
requirement (based on guidelines for horses) and mean concentrations of
excreted microminerals in tapir feces.


Zn Cu*


mg-kg-1


Tapir food
Browse


Mean
SD


454.49
471.61


32.30
39.36


7.15
6.46


348.94
290.34


14.91
9.87


Fruits


Mean 42.98
SD 52.89


Required1
Maintenance
Growth
Females2

Tapir feces


Mean
SD


40.00
40.00
40.00


202.04
151.34


22.45 10.55 70.48 14.33
7.39 5.56 62.44 0.65


40.00
40.00
40.00


10.00
10.00
10.00


40.00
50.00
50.00


Unknown


85.54 42.86 2952.15
91.12 68.25 11767.28


1 Suggested requirements for horses (NRC 1989).
2 Suggested requirements for pregnant and lactating females (NRC 1989).
* Copper requirements for tapirs may be much higher than requirement for horses
(Janssen et al. 1999).