Citation
Ecology and Impacts of Introduced Non-Human Primate Populations in Florida

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Title:
Ecology and Impacts of Introduced Non-Human Primate Populations in Florida
Creator:
Anderson, Carolyn Jane
Place of Publication:
[Gainesville, Fla.]
Florida
Publisher:
University of Florida
Publication Date:
Language:
english
Physical Description:
1 online resource (120 p.)

Thesis/Dissertation Information

Degree:
Doctorate ( Ph.D.)
Degree Grantor:
University of Florida
Degree Disciplines:
Interdisciplinary Ecology
Committee Chair:
JOHNSON,STEVEN A
Committee Co-Chair:
HOSTETLER,MARK E
Committee Members:
ANDREU,MICHAEL G
HEARD,DARRYL J
PINE,WILLIAM E,III
Graduation Date:
12/17/2016

Subjects

Subjects / Keywords:
Animals ( jstor )
Bird nesting ( jstor )
Humans ( jstor )
Monkeys ( jstor )
Population estimates ( jstor )
Population growth ( jstor )
Population size ( jstor )
Primates ( jstor )
Species ( jstor )
Wildlife management ( jstor )
Interdisciplinary Ecology -- Dissertations, Academic -- UF
conservation -- florida -- invasive -- macaque -- management -- monkey -- wildlife
Silver Springs State Park ( local )
Genre:
bibliography ( marcgt )
theses ( marcgt )
government publication (state, provincial, terriorial, dependent) ( marcgt )
born-digital ( sobekcm )
Electronic Thesis or Dissertation
Interdisciplinary Ecology thesis, Ph.D.

Notes

Abstract:
Three species of non-human primates have successfully established populations in Florida: squirrel monkeys (Saimiri sp.), vervet monkeys (Chlorocebus sabaeus), and rhesus macaques (Macaca mulatta). In this study I sought to validate and synthesize the history and status of introduced populations of non-human primates in Florida using literature review, content analysis of popular media, and expert interviews. I then sought to evaluate the potential environmental impacts, current population size, and projected population growth of the oldest and largest population of non-human primates in Florida, the rhesus macaques of Silver Springs State Park (SSSP). At least five populations of squirrel monkeys have established in Florida since the 1960s; only a single dwindling population remains. A single population of vervet monkeys established in Dania Beach in the 1950s, but has demonstrated little change in population size over the past 20 years. A population of rhesus macaques was established in Titusville from the 1970s through 1990s. Another population of rhesus macaques was established in two islands in the Florida Keys from the 1970s-2000 and was removed after causing extensive environmental damage. The rhesus macaque population in SSSP was established in the 1930s, and despite the removal of ~1,000 individuals between 1984-2012, remains the largest population of introduced non-human primates in Florida. The rhesus macaques in SSSP consumed 21 of 100 artificial nests placed in their habitat, indicating they may depredate nests of native breeding birds. Radio collar data from December 2014 through February 2015 indicated this population selects floodplain swamp habitat. The winter home range was estimated to be 0.65 km2 using a 95% kernel density estimate and 1.26km2 using a minimum convex polygon estimate. The Fall 2015 population estimate included 176 rhesus macaques among five groups, and our models projected this population will double by 2022. Models suggested it may be possible to eradicate this population through culling, and the population could be maintained or reduced through sterilization. Given the pervasive population growth, management intervention will likely be necessary to eliminate or reduce the environmental and human health risks of this population. ( en )
General Note:
In the series University of Florida Digital Collections.
General Note:
Includes vita.
Bibliography:
Includes bibliographical references.
Source of Description:
Description based on online resource; title from PDF title page.
Source of Description:
This bibliographic record is available under the Creative Commons CC0 public domain dedication. The University of Florida Libraries, as creator of this bibliographic record, has waived all rights to it worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law.
Thesis:
Thesis (Ph.D.)--University of Florida, 2016.
Local:
Adviser: JOHNSON,STEVEN A.
Local:
Co-adviser: HOSTETLER,MARK E.
Statement of Responsibility:
by Carolyn Jane Anderson.

Record Information

Source Institution:
UFRGP
Rights Management:
Copyright Anderson, Carolyn Jane. Permission granted to the University of Florida to digitize, archive and distribute this item for non-profit research and educational purposes. Any reuse of this item in excess of fair use or other copyright exemptions requires permission of the copyright holder.
Classification:
LD1780 2016 ( lcc )

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ECOLOGY AND IMPACTS OF INTRODUCED NON HUMAN PRIMATE POPULATION S IN FLORIDA By CAROLYN JANE ANDERSON 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 2016

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2016 Carolyn Jane Anderson

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To my aunt, Dr. Melissa Keller, one of the kindest, strongest and most generous people I know. I am forever grateful for your love and guidance.

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4 ACKNOWLEDGMENTS I first thank my advisers, Dr. Steve Johnson and Dr. Mark Hostetler, who encouraged me to take and treated me with unrelenting patience along the way. I am so grateful for the time, enthusiasm, and dedication of my committee members Dr. Darryl Heard, Dr. Bill Pine, and Dr. Michael Andreu. They stuck by this e ver changing and often unpredictable project. The success of a graduate student largely lies in the hands of those who guide them, and I am fortunate to have followed these five exemplary leaders. I give my sincerest gratitude to Mickey Summers, my projec t consultant and constant enthusiasm not only made this project possible, but also made it fun. I am proud to call Mickey and Rayne my friends. I thank the administrativ e and operations staff of WEC and SNRE: Elaine, Kelley, Caprice, Monica, Claire, Fiona, Sam, Kyle, Heather, Karen, and Cathy. They are the support system that makes our research possible. I am so grateful for the encouragement and advice of Dr. Mike Moult on. He taught me to enjoy the ride, do my best, and not take myself too seriously. I also thank Dr. Christina Romagosa, who guided me with kindness and expertise when things got tricky. I thank Sally Lieb, manager of Silver Springs State Park, as well as t he staff of Silver Springs State Park, for allowing me to conduct this work in their beautiful park. This project sometimes made thei r jobs more difficult, but they always treated me respect, encouraged me to keep going, and provided me with informatio n wh ich was critical to allow me to start t o understand the macaques. I also thank Kristen Sommers

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5 of the FWC for providing the equipment, information, and support that was essenti al to our success. I give m any thanks go to Bob Gottschalk, who helped me learn the ways of the macaque. I am so grateful for the many hours he volunteered on the project and his support throughout the process. I am so grateful for our funders: The USDA, The Felburn Foundation, FWC, and the USGS. I appreciate them taking a chance on a graduate student. I truly appreciate the professionals and faculty members outside of my committee who helped me design and/or analyze my data: Dr. Katie Sieving, Dr. Theron Terhune, Dr. Mathieu Basile, Dr. Madelon van de Kerk, Mr. James Colee and Mr. K e Zhang. I also thank Dr. Marty Main for loaning me equipment critical to the success of this project. I thank Missy Williams and Dr. Linda Taylor for providing me with important information about the monkey populations of south Florida. I thank the many folks who spent time volunteering on this research, especially Brittany Bankovich and Lauren Gawel. I th ank the brilliant Buddy Hyde for building our amazing camouflage blinds. I thank my amazing friends Heather Moylett Liz Dodson, and Becky Lintz They kept my head straight and reminded me to have fun. They also will never call me Dr. I give a ll my grati tude and love to Jeff, who came in just when I needed him. Finally I thank my family my parents, Mark and Lynne, my sister and brother in law Sarah and Franklin, my brother and sister in law Steve and Lindsay, my brother Xavier, and my amazing nephews a nd niece Henry, Miles, Evelyn, Oscar and Simon They were my driving force and I hope to make them proud.

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6 TABLE OF CONTENTS page ACKNOWLEDGMENTS ................................ ................................ ................................ .. 4 LIST OF TABLES ................................ ................................ ................................ ............ 8 LIST OF FIGURES ................................ ................................ ................................ .......... 9 ABSTRACT ................................ ................................ ................................ ................... 11 CHAPTER 1 INTRODUCTION TO THE MONKEYS OF FLORIDA ................................ ............. 13 Background ................................ ................................ ................................ ............. 13 Research Objectives ................................ ................................ ............................... 13 2 HISTORY AND STATUS OF INTRODUCED NON HUMAN PRIMATE POPULATIONS IN FLORIDA, U.S.A. ................................ ................................ ..... 16 Introduction ................................ ................................ ................................ ............. 16 Methods ................................ ................................ ................................ .................. 20 Results ................................ ................................ ................................ .................... 22 Data Analysis ................................ ................................ ................................ ... 22 Free Ranging P opulations ................................ ................................ ................ 22 Semi Captive Populations ................................ ................................ ................ 31 Discussion ................................ ................................ ................................ .............. 32 3 PREDATION OF ARTIFICIAL NESTS BY INTRODUCED RHESUS MACAQUES ( MACACA MULATTA ) IN FLORIDA, U.S.A. ................................ ...... 44 Introduction ................................ ................................ ................................ ............. 44 Methods ................................ ................................ ................................ .................. 46 Study Site ................................ ................................ ................................ ......... 46 Study Design ................................ ................................ ................................ .... 47 Analyses ................................ ................................ ................................ ........... 49 Results ................................ ................................ ................................ .................... 49 Discussion ................................ ................................ ................................ .............. 50 4 WINTER HOME RANGE AND HABITAT SELECTION OF AN INTRODUCED POPULATION OF RHESUS MACAQUES ( MACACA MULATTA ) IN FLORIDA, U.S.A. ................................ ................................ ................................ ..................... 56 Introduction ................................ ................................ ................................ ............. 56 Methods ................................ ................................ ................................ .................. 58 Study Site ................................ ................................ ................................ ......... 58

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7 Animal Capture and Collar Placement ................................ ............................. 58 Data Analysis ................................ ................................ ................................ ... 60 Results ................................ ................................ ................................ .................... 61 Discussion ................................ ................................ ................................ .............. 61 5 POPULATION ESTIMATE AND MANAGEMENT OPTIONS OF INTRODUCED RHESUS MACAQUES IN SILVER SPRINGS STATE PARK, FLORIDA, USA ...... 67 Introduction ................................ ................................ ................................ ............. 67 Study Area ................................ ................................ ................................ .............. 67 Methods ................................ ................................ ................................ .................. 72 Population Estimate ................................ ................................ ......................... 73 Model Design ................................ ................................ ................................ ... 73 Model Parameteri zation ................................ ................................ ................... 75 Results ................................ ................................ ................................ .................... 76 Population Estimate ................................ ................................ ......................... 77 Population Modeling ................................ ................................ ......................... 77 Discussion ................................ ................................ ................................ .............. 78 Management Implica tions ................................ ................................ ....................... 79 6 ................................ 97 Macaques and Modern Conservation ................................ ................................ ..... 97 Wildlife Management in Florida ................................ ................................ ............... 98 Human Primate Populations .......................... 99 LIST OF REFERENCES ................................ ................................ ............................. 103 BIOGRAPHICAL SKETCH ................................ ................................ .......................... 120

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8 LIST OF TABLES Table page 2 1 Introduced primate populations in Florida, U.S.A. ................................ .............. 40 3 1 Nest Mortality by Study Site ................................ ................................ ................ 54 3 2 Daily Survival Rate of Depredated Nests by Predator ................................ ........ 54 3 3 Logistic Regression Predicting Proportion of Nests Depredated by Macaques by Macaque Abundance ................................ ................................ ..................... 54 5 1 Number of rhesus macaques observed in two habituated groups at Silver Springs State Park by census and camera trapping ................................ ........... 88 5 2 Minimum number of animals observed via camera traps and estimated total number of animals using observed age specific detection probability of three unhabitua ted groups of rhesus macaques at Silver Springs State Park ............. 88 5 3 Estimated total number of rhesus macaques in Silver Springs Stat e Park, using census values for two habituated groups and estimated values based on detection probability for three unhabituated groups ................................ ....... 89 5 4 Age specific annual survival rates from other rhesus macaque populations ...... 89

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9 LIST OF FIGURES Figure page 2 1 Adult Squirrel Monkey ( Saimiri sciureus ) in Ft. Lauderdale, Florida ................... 41 2 2 One juvenile and two adult Vervet Monkeys ( Chlorocebus sabaeus ) in Dania Beach, Florida ................................ ................................ ................................ .... 41 2 3 One infant and two female adult Rhesus Macaques ( Macaca mulatta ) in Silver Springs, Florida ................................ ................................ ........................ 42 2 4 Approximate locations of introduced non human primate populations in Florida, U.S.A. ................................ ................................ ................................ .... 43 3 1 Locations of the four study sites in SSSP ................................ ........................... 55 3 2 Image captured by a camera trap of a rhesus macaque consuming a quail egg from an artificial nest ................................ ................................ ................... 55 4 1 Winter home range estimates of a group of rhesus macaques in Silver Springs State Park, Florida, U.S.A., using minimum convex polygon and kernel density methods ................................ ................................ ....................... 66 5 1 Locations of camera trap stations in Silver Springs State Park, Florida ............. 90 5 2 Life cycle d iagram and corresponding population matrix for rhesus macaques in Silver Springs State Park. In both the life cycle diagram and the matrix, P x represents the survivorship of each respective age class (P x = infant survivorship, P sa = subadult survivorship, P a = adult survivorship), and F x represents fertility. The solid arrows represent transition between age classes and are labeled with the survival probability for each transition. The dashed arrow represents fertility as a function of adult female survivo rship. Subadults were categorized as yearlings and two year olds and assumed to have equal survivorship; thus, half of subadults were assumed to remain within the age class each year, and half were assumed to become adults. ....... 91 5 3 Projected population growth of rhesus macaques in Silver Springs State Park using reported survival rates from other rhesus macaque populations. Population size was not modeled beyond 400 individuals, as potential carrying capacity beyond this is unknown. ................................ ......................... 92 5 4 Sensitivity and elasticity measurements of infant survival (S i ), subadult survival (S sa ), adult survival (S a ), and fertility (F) of the introduced population of rhesus macaques in Silver Springs State Park, Florida. ................................ 93 5 5 Projected female rhesus macaque population size in Silver Springs State Park, using survivorship rates reported in Hernandez Pacheco et al. (2013),

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10 under four management scen arios culling 50% of subadult and adult females, culling 80% of subadult and adult females, sterilizing 50% of adult females (age 3 and older), and sterilizing 80% of adult females (age 3 and older) and implemented at four levels of frequency annuall y, biannually, every five years, and every 10 years. The point at which the female population (N f ) reaches 234 individuals is noted, as this is where total population (N) reaches 400, and carrying capacity beyond this is unknown. ..... 94 5 6 Woman inciting an aggressive display from an adult female rhesus macaque ( Macaca mulatta ) by attempting to hand feed it in Silver Springs State Park, Florida ................................ ................................ ................................ ................ 96

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11 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 ECOLOGY AND IMPACTS O F INTRODUCED NON HUMAN PRIMATE POPULATIONS IN FLORIDA By Carolyn Jane Anderson December 2016 Chair: Steven Johnson Co chair: Mark Hostetler Major: Interdisciplinary Ecology Three species of non human primates have successfully established populations in Florida: squirrel monkeys ( Saimiri sp. ), vervet monkeys ( Chlorocebus sabaeus ), and rhesus macaques ( Macaca mulatta ). In this study I sought to validate and synthesize the history a nd status of introduced populations of non human primates in Florida using literature review, content analysis of popular media, and expert interviews I then evaluate d the potential environmental impacts current population size, and projected population growth of the oldest and largest population of non human primates in Florida, the rhesus macaques of Silver Springs State Park (SSSP) At least five populations of squirrel monkeys have established in Florida since the 19 6 0s; only a single dwindling popula tion remain s A single population of vervet monkeys established in Dania Beach in the 1950s, but has demonstrated little change in population size over the past 20 years. A p opulation of rhesus macaques was present in Titusville from the 1970s through 1990 s A nother population of rhesus macaques was established in two islands in the F lorida Keys from the 1970s 2000 and was removed after causing extensive environmental damage.

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12 The rhesus macaque population in SSSP was established in the 1930s .D espite the removal of approximately 1,000 individuals from 1984 to 2012 it remains the largest population of introduced non human primates in Florida. The rhesus macaques in SSSP consumed 21 of 100 artificial nests placed in their habitat, indicating they may depredate nests of native breeding birds. Radio collar data from December 2014 to February 2015 indicated one group within this population selects floodplain swamp habitat. The winter home range was estimated to be 0.65 km 2 u sing a 95% kernel density estimate and 1.26km 2 using a minimum convex polygon estimate. The f all 2015 population estimate included 176 rhesus macaques among five groups, and is projected to double by 2022. M odels indicate it is possible to eradicate this p opulation through culling, but the population could also be stabilized or reduced through sterilization Given the projected population growth, intervention will be necessary to eliminate or reduce the environmental and human health risks of this populatio n.

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13 CHAPTER 1 INTRODUCTION TO THE MONKEYS OF FLORIDA Background Humans have intentionally and unintentionally relocated non human primates (hereafter: primates) to novel habitats for at least five centuries. At least ten species of primates have been intentionally and unintentionally introduced in the U.S The impacts of these species have ranged from seemingly innocuous to extremely invasive To date, three species of primates have established populations in Florida: squir rel monkeys ( Saimiri sp. ) vervet monkeys ( Chlorocebus sabaeus ), and rhesus macaques ( Macaca mulatta ). Prior to this study, the history, invasion success, and current status of these species was poorly understood Research Objectives Prior to this study, information on the history and status of introduced primate populations in Florida consisted of local knowledge, word of mouth, and a few out dated websites. It was clear the rhesus macaque population of Silver Springs State Park was the oldest, largest, a nd had received the most publicity T he current population status and potential environmental impacts however, were unknown. In this study I sought to answer f ive questions about introduced primate populations in Florida: 1. How many populations of primate s have been introduced in Florida ? 2. W hat is the current status of these populations? 3. What are the potential environmental impacts of the population of rhesus macaques in Silver Springs State Park? 4. What is the current population size of rhesus macaques in Silver Springs State Park ? 5. H ow will the Silver Springs State Park rhesus macaque population size change in the future?

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14 In Chapter 2 I describe the history and current status of introduced primate populations in Florida. I compiled this information using s ystematic review of published and grey literature, content analysis of popular media, interviews with experts, and site visits of historic and persistent populations. In this chapter I describe populations that have established (reproducing without human i ntervention) or become invasive (established and causing harm to environmental or economic resources or human health; NISC 2006). This chapter is currently under review for publication. In Chapter 3 I discuss the results of a study conducted to evaluate if rhesus macaques in Silver Springs State Park would consume bird eggs placed in artificial nests in their habitat. This study was published in 2016 in Biological Invasions (Anderson et al. 2016) In Chapter 4 I describe the winter home range and habitat us e of a group of rhesus macaques in Silver Springs State Park. This information was obtained through the use was later observed to have healed). Despite our quick response and removal of the collar, we received significant threats from animal rights activists and were forced to discontinue the study. The rapid and extensive response to this incident help ed us gain a better appreciation for the contentiousness of rhesus maca que research and management in Florida It emphasized the difficulties and importance of communicating with the public It has also influenced our management recommendations. In Chapter 5 the f all 2015 population size of rhesus macaques is estimated, as we ll as future population projections under varying management scenarios. In this chapter I compare the projected future population size using either culling individuals or a st erilization program of sexually mature female rhesus macaqu es in Silver Springs S tate Park I

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15 compared the advantages and disadvantages of each option. In Chapter 6 I discuss the over all research future research needs, and my recommendations for future management. This study was conducted pursuant to IACUC permit 201308022, DEP permi t 01281413, and FWC permit EXOT 13 249.

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16 CHAPTER 2 HISTORY AND STATUS OF INTRODUCED NON HUMAN PRIMATE POPULATIONS IN FLORIDA, U.S.A. Introduction Humans have introduced non human primate (hereafter: primate) populations into novel habitats since at least the 16 th century (Long 2003). However, primates are a relatively new invader in the U.S.A. and pose a growing and understudied threat to native flora, fauna, and humans. Since the 1930s at least ten species of primates have been introduced in the U.S.A. ( Dierenfeld and McCann 1999, Engeman et al. 2010, Feild et al. 1997, Gonzlez Martnez 2004, Hall et al. 2007, Hyler 1995, Maples et al. 1976, Mowry et al. 1997, Rawlins and Kessler 1983, Taub and Mehlman 1989, Paterson 1996, Wilson and Elicker 1976, Wolfe and Peters 1987) Some were either unintentional releases or from unknown sources The rational for intentional releases varied from conservation, tourism, to behavioral and/or biomedical research. Although the native ranges of these species vary in climat ic and environmental conditions, successful introductions have been restricted to the southeastern U.S.A. and Puerto Rico. The impacts of these introductions range from seemingly innocuous to extensive environmental destruction and economic loss At least five primate species have been intentionally introduced on barrier islands in Georgia, U.S.A. All were free ranging but provisioned with food and provided veterinary care. The Wildlife Conservation Society began introducing lemurs onto St. Catherines Isla nd in 1984 to study their behavior and support conservation efforts (Dierenfeld and McCann 1999, Hall et al. 2007) Three lemur species were introduced on the island: Blue eyed Black Lemurs ( Eulemur macaco ), Black and White Ruffed Lemurs ( Varecia variegate ), and Ring Tailed Lemurs ( Lemur catta; Yabsley et al. 2007) In 2013 only

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17 Ring Tailed Lemurs remained on the island, including approximately 100 individuals (C. Jane Anderson, pers. observation) Lion Tailed Macaques ( Macaca silenus ) were introduced to St Catherines Island, GA, in 1990 (Mowry et al. 1997), but were subsequently removed after they proved to be aggressive towards humans and predators of native bird nests (Anderson et al. 2016). Between 1972 1973 Yerkes National Primate Research Center relea sed a single adult male and 7 adult female Chimpanzees ( Pan troglodytes ) onto an isolated section of Ossabaw Island, Georgia (Long 2003, Wilson and Elicker 1976) to evaluate the feasibility of establishing a free ranging research colony in a semi tropical environment. A single female infant was born on the island (Wilson and Elicker 1976). After the conclusion of the project, the Chimpanzees were removed and returned to captivity in the mid 1970s (Elizabeth Dubose, Ossabaw Island Foundation, pers. comm.). M acaque species (genus Macaca ) have demonstrated extensive population growth when introduced in the U.S.A. In February 1972 a population of 150 Japanese Macaques ( Macaca fuscata ) was transported from Arashiyama, Kyoto, Japan, to a ranch in South Texas (Fedi gan 1991, Paterson 1996) B y the mid 1990s the population reached over 800 animals and was believed to be causing environmental destruction, including depredati on of native bird eggs (Feild et al. 1997) Funds were raised to capture the animals and move th em to a fenced property in Dilley, TX, where their decedents are now within a sanctuary (Born Free USA Primate Sanctuary 2016). In 1979 over 1,400 Rhesus Macaques ( Macaca mulatta ) were placed on Morgan Island, South Carolina to establish a breeding popula tion for biomedical research (Taub and Me h lman 1989; Klopchin et al. 2008). This population reached nearly 4,000

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18 individuals in the late 1980s (Taub and Me h lman 1989) and was estimated to be approximately 3,000 animals in 2008 (Klopchin et al. 2008). While no environmental impact research has been published from the island, tidal creeks surrounding the island were found to have elevated levels of fecal coliform and E scherichia coli attributed to the macaques (Klopchin et al. 2008). In December 1938, 409 Rhesus Macaques and 14 Gibbons ( Hylobates sp. ) were released on Cayo Santiago, a 15.2 ha island off the eastern coast of Puerto Rico, to develop a colony for behavioral research and to provide healthy, accessible animals for biomedical research ( Rawlin s and Kessler 198 3 ). The Gibbons proved aggressive to the Macaques and humans (Rawlins and Kessler 1983, Wilson and Elicker 1976) and were subsequently removed in 1941 (Rawlins and Kessler 1983). The Rhesus Macaques have been maintained for behaviora l, physiological, demographic, ecological and non invasive biomedical research and are provisioned daily with food (Hernndez Pacheco et al. 2013, Hernndez Pacheco et al. 2016). Despite removal of over 4,000 individuals from 1984 to 2012 (Hernndez Pachec o et al. 2016), the 2016 population was over 1,550 (Angelina Ruiz Lambides, University of Puerto Rico, pers. comm.). The most widespread and destructive introduction of primates within the U.S.A. thus far is of Rhesus Macaques and Patas Monkeys ( Erythroceb us patas) in southwestern Puerto Rico and Desecheo Island. The m acaques were introduced onto what is today Desecheo Island National Wildlife Refuge, off the western coast of Puerto Rico, in 1966 to study behavioral adaptations to a novel environment (Engem an et al. 2010, Evans 1989) Prior to the introduction of m acaques, the island provided habitat for thousands of pairs of breeding seabirds S eabird nesting began declining after the introduction of

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19 rats in the early 1900s and completely halted by 1970 after the added pressure of nest predation from the macaques (Evans 1989) In the early 1960s Rhesus Macaques were introduced to the islands of Cueva and Guayacn, Puerto Rico, through a collaborative project between the National Institute of Health and the Caribbean Primate Research Center. Shortly after their introduction to the islands, the animals began escaping onto mainland Puerto Rico. Despite the escapes, the Caribbean Primate Research Center an d Federal Drug Administration continued releasing Rhesus Macaques on the islands through the 1970s; from 1971 1979 46 Patas Monkeys were added to the islands (Gonzlez Martnez 2004) In subsequent decades both species were able to spread to the mainland and increase in population size, causing substantial damage to the agricultural industry through crop raiding. In 2008 the U.S. Department of Agriculture (USDA) estimated annual damages to be $300,000 in direct losses and over $1 million in management cos ts (USDA 2008). The Puerto Rico Department of Environment and Natural Resources and USDA began a collaborative effort to control the population in 2008 and by 2014 had euthanized over 5,000 monkeys (Lpez Ortiz 2014). Three species of primates have establi shed populations in Florida, U.S.A.: Squirrel Monkeys ( Saimiri sp.; Fig. 2 1), Vervet Monkeys ( Chlorocebus sabaeus; Fig. 2 2), and Rhesus Macaques (Fig. 2 3). Very little research has been conducted or published on these populations. M ost information has b een generated through popular media reports, grey literature, and word of mouth. Given the potential for primate populations to thrive in novel habitats and threaten environmental and economic resources, it is critical to understand their historic and curr ent status The aim of this study was to compile,

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20 validate, and synthesize information on historic and extant free ranging primate populations in Florida and to understand variations in success among these populations. For each population, we sought to det ermine: 1) introduction date and source; 2) whether there have been management efforts to increase or decrease the population; 3) for those no longer extant, how long the population survived and why it is no longer in existence; 4) for extant populations, current population size and potential impacts. Methods We used four methods to assemble data on the history and current status of primate populations in Florida: 1) systematic review of peer reviewed and grey literature; 2) content analysis of popular media; 3) semi structured interviews with local experts and 4) site visits of reported historic and extant populations. We conduc ted a systematic review of peer reviewed and grey literature using the framework described by Pullin and Stewar t (2006). We defined our geographic range as the state of Florida and used relevant search terms to query Web of Science and Google Scholar for peer reviewed articles and abstracts. We used the search function in Google to locate grey literature. We included all peer reviewed articles, state agency reports, university theses, book chapters, and conference abstracts pertaining to introduced populat ions of primates in Florida. We conducted a content analysis (Riffe et al. 1998) of news articles to synthesize information on introductions, population estimates, and management efforts of introduced populations of primates in Florida. To compile news art icles we used the introductions, as well as the common name of each species with their known introduced

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21 r articles by individuals and special interest groups were excluded Further, we used only articles referencing primate populations and not free ranging individuals. Concur rent with the literature review and content analysis of media reports, we conducted semi structured interviews with biologists, land managers, and local experts (n = 19). Interviews were conducted between July 2013 and May 2016. Initial interviewees were s elected based on their knowledge and experience in the respective location, and subsequent interviewees were selected through snowball (Goodman 1961) and respondent driven sampling techniques (Heckathorn 1997) Interview s personal experience with local primate populations, length of time local populations were or have been established, whether any local management regimens were currently or historically used to control introduced primate populations, and what local opinio ns and perceptions were of the respective primate population. From June 2014 to February 2016 we conducted site visits of locations of reported historic and current primate populations. For populations found to be extinct, we interviewed local experts and residents to determine the last time primates were observed and variations in population size prior to extinction. For extant populations, we interviewed local residents and experts, and we observed the animals to estimate minimum population sizes. Observ ations of Rhesus Macaques in Silver Springs were conducted concurrently with other research (e.g., Anderson et al. 2016) from January 2013 December 2015.

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22 Results Data Analysis We reviewed 13 peer reviewed articles, 3 university theses, 2 book chapters, 2 peer edited articles, and 2 conference abstracts. Most of these (n = 8) focused on the Rhesus Macaques of Silver Springs (Hammond 1989, Maples et al. 1976 Peters 1983 Riley and Wade 2016 Sarris 1980 Wolfe and Peters 1987 Wolfe 1986, 2002) or on the R hesus Macaques in the Florida Keys (n = 6; Johnson 1989; Johnson and Kapsalis 1995, 1998; Kruer 1996; Lehman et al. 1994; Taylor et al. 1994). Five publications describ ed Squirrel Monkey introductions including 3 populations (Elgart 2009, Layne 1969, Leon 1997, Taylor and Lehman 1997, Wheeler 1990), and only two publications document ed Vervet Monkeys (Hyler 1995, Williams 2015). One book chapter describ ed all three species (Layne 1997). We revi ewed 106 popular media articles published from 1960 to 2016. Most articles were about Rhesus Macaques in Silver Springs (n = 32) or the Florida Keys (n = 22), and only two describ ed Rhesus Macaques in Titusville. Rhesus Macaque news articles ranged from 1977 2016. We analyzed 18 article s about Vervet Monkeys dating from 1983 to 2015. Nearly one third of articles reviewed (n = 32) described Squirrel Monkey populations in Naples, Boca Raton, Ft. Lauderdale, and Lake Wales; no news articles were found describing Squirrel Monkeys in Silver S prings. Free Ranging P opulations Squirrel m onkeys Based on our review, there have been at least five established Squirrel Monkey populations in Florida (Table 2 1; Fig. 2 4). Squirrel Monkeys (genus Saimiri ) are native to Central and South America. Four s pecies primarily occupy tropical lowland forests throughout the Amazon basin T he Central American Squirrel Monkey

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23 ( Saimiri oerstedii ) however, is native to forests along the Pacific Coast of Costa Rica and Panama. Among neotropical primates, Squirrel Mon keys are considered habitat generalists, with the capacity to survive in disturbed and edge forests (Kinzey 1997). They are primarily frugivorous and insectivorous, but will supplement their diet with other plant parts, eggs, and small invertebrates and ve rtebrates (Baldwin 1985, Kinzey 1997). Of the five Squirrel Monkey populations introduced in Florida, four are extinct. A dwindling population remains on the Squirrel Monkey population on the Bartlett Estate is uncertain; Wheeler (1990) suggested the population came from two pairs released from captivity in a local bar in the 1970s Leon (1997) and Taylor and Lehman (1997) however, suggest ed the population est ablished on the property in the 1940s. Researchers consistently identified this population as the common Squirrel Monkey, Saimiri sciureus (Leon 1997, Taylor and Lehman 1997, Wheeler 1990). T he population was reported to be 43 individuals in 1988 (Wheeler 1990) and 39 individuals in 1995 to 1996 (Leon 1997). The animals are not confined to the property; researchers from the 1990s routinely observed monkey s traveling into the nearby Hugh Taylor Birch State Park (Linda Taylor, University of Miami, pers. comm.). During our site visit in 2014, there were only three monkeys remaining on the property. S taff reported seeing dead animals during particularly cold winters in 2009 and 2010. Researchers from the 1990s confirmed a trapper was removing animals from the perimeter of the property during the time of their observations. This was perhaps for sale into the pet industry (Linda Taylor, University of Miami, pers. comm.) a very lucrative endeavor (Darryl Heard, UF College

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24 of Veterinary Medicine, pers. comm) It is unknown how many animals were trapped and removed. At the time of our visit the animals were provisioned daily with food and fresh water. Squirrel Monkeys are reported to have established around 1960 in what is today Silver Spring s State Saimiri occurred in this population (Maples 1976). The animals were initially contained within an enclosure near the headspring, but were later intentionally released into the surrounding forests (Michael Summ ers, Silver Springs State Park pers. comm., Maples et al. 1976). In 1961 the population numbered approximately 12 to 15 animals (Layne 1969). Tourists frequently hand fe d the animals (Michael Summers, Silver Springs State Park, pers. comm.). They were no longer in the park by the early to mid 1970s (Maples et al. 1976). The reason for their disappearance is uncertain. Maples (1976) reported the animals may have moved towards the Ocklawaha River, and it is likely they did not survive. It is pos sible they were driven out of the area by introduced Rhesus Macaques (see below), as Rhesus Macaques are aggressive and prone to attack unfamiliar conspecifics (Maestripieri and Hoffman 2012). The establishment date and source of Squirrel Monkeys in Master piece Gardens Saimiri within this population is also unclear. The earliest record of the population we located was from 1971 (Florida State Library & Archives 2016), sug gesting the population may have established in the 1960s. It is unclear whether the introduction of these animals was intentional. A 1981 news article stated the owner of the property was attempting to trap the animals to sell them at auction (Bair 1981) W e were unable

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25 however, to obtain records on the success of this trapping effort. Another local newspaper article from 1983 reported the population was dwindling and suggested predation and cold weather were the primary causes (Bair 1983). Property manage rs reported occasionally hearing monkeys in the surrounding forests in the late 1980s. In the winter of 1989 dead monkeys were found on the property; there have been no reported observations since that time (Paula Blackburn, Masterpiece Gardens, pers. comm .) No formal population estimates were published during the approximately 20 year span of this population. News articles suggested there were hundreds of animals (Bair 1981, 1983) T hese numbers however, should be considered with caution as untrained observers have been found to overestimate primate population sizes (Malaivijitnond et al. 2011). A population of Squirrel Monkeys was previously established along the Gordon population was confirmed to be Saimiri sciureus (Alison Elgart, Florida Gulf Coast University, pers. comm.). City records indicate the population established in the 1960s (City of Naples 2012) however t he exact establishment date and source are unknown. I n the late 1990s to the early 2000s several reports were made of individuals trapping the monkeys, potentially for the pet trade or research industry. In 2002 city council members proposed a local ordinance to protect the monkeys from trapping, but the ord inance was denied in 2003 (City of Naples 2012). In 2009 the population consisted of only an adult male, a juvenile male, and a female that was either a juvenile or adult (Alison Elgart, Florida Gulf Coast University, pers. comm.) occupying an area of

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26 appr oximately 4.77km 2 (Elgart 200 9 ). There have been no reported sightings since approximately 2010 (Jeff Schmid, Conservancy of Southwest Florida, pers. comm.). In 1970 a captive colony of Squirrel Monkeys on the campus of Florida Atlantic University was rel eased by animal rights activists (FAU 2016, Tarrant 1976). The animals persisted as a free ranging population on the campus, with some supplemental provisioning. The release was believed to include around 65 animals. By 1976 the population was reported to include only 3 animals (Tarrant 1976); we did not locate any records of the population after this date. Vervet m onkeys To date there has only been one reported established population of Vervet Monkeys in Florida (Table 2 1; Fig. 2 4). The common name ver six species within the genus Chlorocebus (Haus et al. 2013) Spanning across sub Saharan Africa, the vervets are one of the most widespread genera of primates (Wolfheim 1983). They are habitat generalists and generalist omnivores, which allows them to thrive in a variety of environments. They readily adapt to human settlements in rural, suburban, and urban settings. Across much of their native range they are regarded as pests due to raiding crops (Hill 2000, S aj et al. 2001) and stealing food from homes and trash bins in villages (Long 2003, Fourie et al. 2015) .This h as led to extermination programs in many countries (Long 2003). Vervet Monkeys were introduced into Dania Beach, south of Ft. Lauderdale, in the either escaped or were intentionally released from the Anthropoid Ape Research Foundation, a facility which imported primates for biomedical research (Williams 2015); the number

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27 of ani mals originally released is unknown. I n the early 1990s there were approximately 36 Vervet Monkeys split between two groups (Hyler 1995). In 2015 the population was estimated to be 35 animals split between four groups (Williams 2015). Hyler (1995) reporte d the animals were Chlorocebus aethiops or a hybrid M ore recent evidence suggests they are likely Chlorocebus sabaeus (Deborah Williams, Florida Atlantic University, pers. comm.). In 2013 a group of two or three Vervet Monkeys separated from the main population in Dania Beach and moved south into Miami Dade County. The Florida Fish and Wildlife Conservation Commission trapped a Vervet Monkey, believed to be one of the separated individuals, approximately 33 miles south of Dania Beach and placed it with an individual permitted to hold captive primates T he fate of the other animal(s) is unknown. Aside from the capture of the individual animal, there have been no efforts by the state to control the Vervet Monkey population (Jennifer Ketterlin Eckles, Environmentally Endangered Lands Program, pers. comm.). A 2013 news article (Nolin 2013) stated around seven Vervet Monkeys had been trapped and sold in the early 1990s. There are reports several of the monkeys were trapped in the early 2000s by a private citizen for sale into the biomedical industry, but there are no reports of trapping since then The animals in this population are extremely habituated to humans and have extensive support from the local community (Deborah Will iams, Florida Atlantic University, pers. comm.). Local officials considered a local ordinance to protect the monkeys but to date no policies have been implemented (Jennifer Ketterlin Eckles, Environmentally Endangered Lands Program, pers. comm.).

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28 Rhesus m acaques From our review, three populations of Rhesus Macaques have established in Florida (Table 2 1; Fig. 2 4). Native throughout eastern and southern Asia, Rhesus Macaques are believed to have the largest native range of any non human primate (Southwick et al. 1996). They are habitat generalists, as evidenced by elevations in their native range varying from sea level to 2000m on average (Fooden 2000) They are both arboreal and terrestrial, generalist omnivores, and capable of adapting to a diversity of environmental conditions. Rhesus Macaques are noted human commensals (Richard et al. 1989) with population densities averaging 37.2/km 2 in forested habitats and 201.1km 2 in urban areas and temples (Fooden 2000) Rhesus Macaques represent the oldest, most widespread, and largest of introduced primate species in the U.S.A. A population of Rhesus Macaques established in Titusville in 1976 when they either escaped or were intentionally released from the tourist attraction Tropical the initial introduction. The animals occupied a wooded area near the attraction after their escape (Layne 1997). A 1977 news article suggested there were 35 to 75 animals and state wildlife officia ls planned to trap and remove them (Zimmerman 1977) N o state records however, confirm or deny whether this occurred. In the early 1980s an individual trapped approximately six Rhesus Macaques from Titusville and released them into the area occupied with an established Rhesus Macaque population in Silver Springs (Mike Legare, US Fish and Wildlife Service, pers. comm.) I t is unknown if these animals survived. A 1987 article repor ted the monkeys in Titusville harassed motorists

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29 (Rose 1987). The last reported observation of Rhesus Macaques in Titusville was in the early 1990s (Layne 1997). In 1973 Charles Rivers Laboratories, a subsidiary of Bausch and Lomb, introduced over 1200 f emale and 150 male Rhesus Macaques to Key Lois (historically Loggerhead Key), a 39 ha island in the Florida Keys. From 1978 to 1980 the company moved over 500 of the animals to Raccoon Key, an 81 ha island 15km north of Key Lois (Johnson and Kapsalis 1998, Lehman et al. 1994) The company acquired the islands to develop a breeding colony of Rhesus Macaques for biomedical research. The animals were provisioned daily with food and provided with veterinary care The population on each island quickly increase d with 1,524 births recorded on the islands from 1988 to 1990 (Lehman et al. 1994). It is believed the animals were free of predators on Key Lois, but may have experienced some mortality due to eastern diamond backed rattlesnakes ( Crotalus adamanteus ) on Racc oon Key (Johnson and Kapsalis 1998) Both islands were predominately vegetated by red mangroves ( Rhizophora mangle ) and black mangroves ( Avicennia germinans ). The macaques consumed the new growth of these trees, which was reported to have led to the destru ction of over 30 acres of red mangroves on Key Lois (Kruer 1996) and potentially decreased bird populations on Raccoon Key (Enge et al. 2002). Controversy ensued as environmental activist organizations, including the Audubon Society, called for a removal of the animals from both islands. The State of Florida brought a regulatory action against Charles Rivers Laboratories in 1988 as a result of the environmental damage on the islands, and civil litigation followed (State of Florida 1988, 1992). An agreed Fi nal Judgment was entered following mediation in

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30 1992, wherein the company agreed to remove all Rhesus Macaques and give the deed of Key Lois to the state of Florida by 2013, and remove all macaques from Raccoon Key and give the island to the federal govern ment to be included in the National Wildlife Refuge System by 2014. The order also stated the company must refoliate the islands with mangroves, monitor fecal coliform levels in the waters around the islands, and pay the state $75,000 for damages (State of Florida 1992). The macaques were removed from the islands from 1999 2000. In 2003 Charles Rivers Laboratories and the State of Florida signed a Settlement Agreement, wherein it was agreed the company had met its aforementioned requirements and would also Conservation Trust (State of Florida 2003). The oldest and present ly the largest population of primates in Florida is the Rhesus Macaques in Silver Springs State Park (SSSP), C entral Florida. The population was introduced in the mid 1930s when a glass bottom boat captain placed a small number of Rhesus Macaques on an island in the Silver River to increase tourism. It is unclear how many he released, but a local report in 1938 speculated there were six in the park (Wolfe and Peters 1987). Rhesus Macaques are proficient swimmers, and they promptly swam from the island to the mainland. The monkeys proved popular among tourists, and managers of the tourist attraction purchased and released a pproximately six additional animals aro und 1948 (Wolfe and Peters 1987). A 1968 study estimated the population had grown to 78 individuals spread between two groups (Maples et al. 1976) By 1979 the population was in excess of 150 animals (Sarris 1980). By the mid 1980s the macaque population h ad gro wn to nearly 400 animals in SSSP and had spread to adjacent forests along the Ocklawaha River and in the Ocala National Forest.

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31 In 1984 short term trapping was initiated to reduce the population ; approximately 225 were captured and sold for biomedical research (Wolfe 2002). This practice incited extensive public controversy and protest and was subsequently halted. In the following years, approximately 60 individuals were removed without permit and others were sent to a zoological park (Wolfe and Peters 1987). While specific removal records were not maintained, Wolfe (2002) estimated 500 macaques were removed between 1984 and 1993. In the late 1980s, 13 female macaques were sterilized by hysterectomy in an effort to decrease population growth (Wolfe 2002) From 1998 to 2012 a private trapper, permitted by the state, captured approximately 830 Rhesus Macaques between SSSP and lands along the adjoining Ocklawaha River approximately 630 of which were f rom SSSP and also sold these animals to biomedical research facilities (State of handedly controlled this population in a habitat where they have few terrestrial predators and have previously exhib ited substantial population growth. In 2012 this trapping effort was halted after extensive pressure from the public and special interest groups. A spring 2013 study estimated the population to be 118 individuals (Riley and Wade 2016) The estimated popul ation in f all 2015 was approximately 175 macaques in SSSP (C. Jane Anderson personal observation ) and unknown along the Ocklawaha River. Semi Captive P opulations In 1933 researcher Joseph DuMond introduced six Long Tailed Macaques ( Macaca fascicularis ) into a dense forested area near Miami with the intentions of studying the animals in a natural habitat; the animals were later moved to a fenced enclosure. The facility became a tourist attraction known as Monkey Jungle, working in conjunction with the 50 1(c)3 organization the DuMond Conservancy. The facility

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32 currently houses approximately 20 primate species. Most are captive but three species are semi free ranging : Long Tailed Macaques, Squirrel Monkeys ( Saimiri boliviensis peruviensis ), and Brown Tufte d Capuchins ( Sapajus apella ; Sian Evans, Du M ond Conservancy, pers. comm.) In 2016 there were approximately 110 Long Tailed Macaques, all descendents of the original six (DuMond Conservancy 2016). The semi free ranging animals are in electrified, fenced f orested areas lacking roofs. The tree canopy is trimmed around the fence ( Sian Evans, Dumond Conservancy, pers. comm. ) in an effort to prevent the animals from escaping over the fence. A hotel in Homosassa, Homosassa Riverside Resort, maintains a small is land with Spider Monkeys (genus Atel es ) in the Homosassa River. Water is frequently used to contain captive Spider Monkeys, as these animals do not readily swim (Darryl Heard, UF College of Veterinary Medicine, pers. comm.). The island is situated so patro ns of hotel staff. In spring 2016 there were five Spider Monkeys on the island, one of which was born there There were previously two Squirrel Monkeys (genus Saimiri ), which appeared to have died of natural causes. The island was originally planted with palm trees, which died after the monkeys foraged them; cedar trees now grow on the island (Homosassa Riverside Resort 2016). Discussion Non native species may be cate gorized along a gradient of introduced, to established, to invasive (Colautti and MacIsaac 2004, Lockwood et al. 2007) The three species of primates with reported populations in Florida Squirrel Monkeys, Vervet Monkeys, and Rhesus Macaques span this s pectrum. Despite having the most reported populations throughout the state (n = 5), Squirrel Monkeys have demonstrated

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33 the least success in Florida. Although the Vervet Monkey population in Dania Beach has persisted for several decades, it has changed very little in size. Rhesus Macaques have demonstrated a propensity for survival and population growth in both the Florida Keys and central Florida. Variation in persistence among the primate species in Florida may be attributed to disparities in human interv ention. Trapping and removing animals can decrease population growth or survivorship. Conversely, provisional feeding by humans allow s some populations to persist and/or grow. Provisional food is usually caloric ally rich available in larger proportions (t herefore requiring less energy expenditure), and more predictable than natural foods C onsequently it decrease s generation time, increase s survivorship, and increase s population sizes and densities among primates (Sengupta et al. 2015) Ecological factors may also explain variation in survivorship, such as tolerance of novel environmental resources and climate, ability to survive in human dominated landscapes, tolerance of genetic depression, and capacity for interspecific competition (Lockwood et al. 2007) Despite some reproductive success, Squirrel Monkey populations have never survived more than a few decades in Florida. Trapping and removal likely decreased the Ft. Lauderdale population (Linda Taylor, University of Miami, pers. comm.) and may have influ enced the extinction of the Naples and Masterpiece Gardens populations; we are not aware of any trapping efforts for the other 2 populations. Only t he population in Ft. Lauderdale is reported to have had daily provisional feeding, which may have allowed it to persist longer than other s in Florida.

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34 Inability to tolerate cold temperatures may have limited Squirrel Monkey survival in Florida. Squirrel Monkeys are susceptible to cold stress and have been observed to experience eye, nose, and respiratory impacts when housed in settings with low relative humidity (Abee 1985). Ambient temperature of 26 27C (78.8F 80.6F) is believed to be the lower critical temperature, or temperature below which an individual must use energy above its normal metabolic rate, fo r Squirrel Monkeys (Adair 1985). Squirrel Monkeys housed in outdoor captive settings in Florida must have supplemental heating during winter and sometimes experience frostbite of the extremities (Darryl Heard, UF College of Veterinary Medicine, pers. comm) In Ft. Lauderdale employees reported finding dead Squirrel Monkeys during a particularly cold winter in 2009 2010. This corresponds with the last observations of the Squirrel Monkeys in Naples in 2010. In Florida, t he average temperature from December 2009 to February 2010 was 12. 9 C (Southeast Regional Climate Center 2016) This was significantly lower than the historical average winter temperature from 1895 to 2016 of 14.8C (1. 4 C; Southeast Regional Climate Center 2016). The average winter temperatures in the late 1980s, when Squirrel Monkeys succumbed to cold weather in Polk County (Paula Blackburn, Masterpiece Gardens, pers. comm.), were consistent with the historic average (Southeast Regional Climate Center 2016). If winte r climate extremes did increase Squirrel Monkey mortality, it is possible animals succumbed both to sustained cold periods and to acute, extreme ly cold events. The stability of the Vervet Monkey population in Florida is surprising given this species ha s de monstrated increased population densities in areas with human provisioned food (Brennan et al. 1985, Saj et al. 1999) and there has been little

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35 documented trapping pressure. The persistence of the population over several decades confirms there is reproduct ion and suggests they are capable of surviving in the local climate. It is unlikely population growth is limited by density in Florida, as Vervet Monkey populations over 200/km 2 have been reported (Harrison 1983, Pasternak et al. 2013) It is possible a ge netic bottleneck due to a small founder population and lack of immigration may be precluding population growth (Kolbe et al. 2004, Lee 2002) The small and seemingly stable population size suggest s it has experienced fewer negative impacts than other Verve t Monkey populations, both native and introduced. T he economic damage and human conflict of a n introduced population of Vervet Monkeys in the Caribbean (Dore 2013), coupled with the ir ability predate nests (Patterson et al. 2016) and carry zoonotic pathoge ns (Legesse and Erko 2004) indicate, however, the Florida population must be regularly evaluated Rhesus Macaques have demonstrated appreciable population growth throughout their introduced range in the U.S.A. (Evans 1989, USDA 2008). This is likely a prod uct of their plasticity in environmental requirements (Fooden 2000). The growth of the SSSP population despite a small founder population (n to genetic depression. We are not aware of any introduced populations of Rhesus M acaques that have failed to survive in introduced habitats without human intervention. Thus, the vague data on the management of the population in Titusville limits important insights into invasion ecology, emphasizing the importance of monitoring and publishing species introductions. The propensity of survival in Rhesus Macaques, and related high population growth rates, may lead to population densities that threaten native natural resources as

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36 well as human health and livelihood. As mentioned, Rhesus Macaques in introduced habitats outside of Florida have increased bacteria loads in water bodies (Klopchin et al. 2008), increased mortality of native birds through nest predation (Evans 1989), and caused substantial agricultural damages (USDA 2008). Litt le research has evaluated potential environmental impacts of introduced primates in Florida. The population of Rhesus Macaques in Silver Springs was found to consume quail eggs placed in artificial nests (Anderson et al. 2016 ) indicating they will consume bird eggs if located in their habitat. Cuban Yellow Warblers ( Setophaga petechia gundlachi ), a mangrove specialist, were absent on Raccoon Key in areas where the mangroves had been destroyed by Rhesus Macaques, and only a few solitary males were located i n areas where mangroves were damaged but still standing (Hoffman 1996) In addition to potential ecological impacts, introduced Rhesus Macaques may threaten public health and safety. From 1977 to 1984 the Florida Fish and Wildlife Conservation Commission (FWC) (formerly Florida Game and Fresh Water Fish Commission ) identified 31 monkey human interactions O f these 23 included human injury ; t he agency stopped maintaining primate conflict reports after this time (Montague et al. 1994) These reports are con cerning for public health because as would be expected, the population of Rhesus Macaques in SSSP and along the Ocklawaha River are antibody positive for Herpes B Virus (Montague et al. 1994) Although extremely rare, transmission from macaques to humans can be fatal (Huff and Barry 2003, Jones Engel et al. 2006) From 2013 2016 there were at least four road mortalities of Rhesus Macaques within ten miles of Silver Springs State Park Because the virus is

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3 7 transmitted through exposure to bodily fluids, these carcasses represent a threat for those charged with their removal. Despite potential ecological and human health risk public support for introduced primate populations in Florida remains high. In 1992, the Ocala S tar Banner, a C entral Over 98% of 625 respondents said (Montague et al. 1994) As previously mentioned, local official s in both Dania 09 to 2012. The story received program The Colbert Report. Developing policies for the captive maintenance of non na tive and potentially invasive species is difficult and controversial. In Florida, Vervet Monkeys and macaques are listed as Class II wildlife, indicating they pose a potential threat to people. Individuals wishing to keep these animals in captivity must ob tain a Class II permit, which requires previous experience with the species as well as specific caging and facility requirements. Squirrel Monkeys are classified as a Class III wildlife species, which requires a permit for possession but with fewer restri ctions than a Class II species. In June 2016, there were approximately 225 commercial facilities (e.g., zoos, animal trainers) permitted to keep primates for commercial use A further approximately 450 individuals were permitted to keep captive primates fo r personal use (State of

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38 Florida 2016 1 ). The p otential for escape of these animals is very concerning, as they potentially could migrate into small, extant populations and increase survival (Brown and Kodric Brown 1977, Lockwood et al. 2005) From 1989 to 2016, the FW C recorded nearly 200 reports of escaped or free ranging primates, including over 250 individual animals; at least 115 were captive escapes and 75 of which were permitted (State of Florida 2016 2 ). Damage from Hurricane Andrew in 1992 led to the escape of hundreds of captive animals. Approximately 170 Rhesus Macaques escaped from the University comm.). Hamadryas Baboons ( Papio hamadryas ) escaped their outdoor h ousing at The Manheimer Foundation, a research facility in Florida City, FL. Long Tailed Macaques escaped from both The Manheimer Foundation and from Monkey Jungle (Linda Taylor, University of Miami, pers. comm.). Intensive dart and recapture efforts were initiated to return the macaques to The Manheimer Foundation and Monkey Jungle M ost returned to both sites without intervention but some may have died from storm related trauma (Linda Taylor, University of Miami, pers. comm.) and some are reported to hav e been euthanized (Darryl Heard, UF College of Veterinary Medicine, pers. comm). It is fortunate these animals were unable to establish free ranging populations, as this species has caused extensive environmental ( Safford 2011) economic, and public health threats throughout their introduced range (Lowe et al. 2000). We provide the first comprehensive review of introduced primate populations in Florida, U.S.A. Managers and researchers of invasive species must understand how to classify individual population s as simply introduced rather than invasive, and for those

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39 classified as invasive, how to designate threat levels (Colautti and MacIsaac 2004) We recommend management of Rhesus Macaques be prioritized over the other two introduced primate species in Flori da This is because they have demonstrated faster population growth as well as posing a more immediate and obvious environmental, economic, and public health threat. Historic invasions can be an important predictor of future invasions (Kolar and Lodge 200 1; Hayes and Barry 2008), and successful primate introductions have largely been limited to Old World species (Leon 1997). C hanging climate and landscapes however, may allow successful introduction of new primate species, especially synanthropes. Establis hed primate populations have caused environmental, economic, and human health threats on at least three continents. T he charismatic nature of these species however, makes public support of management programs challenging Futher, primates are of important cultural and religious significance in many countries (Radhakrishna et al. 2013). Managers of areas that experience primate introductions in the future must act quick ly to control them in an ethical manner sensitive to the sentiments of local communities and stakeholders.

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40 Table 2 1. Introduced primate populations in Florida, U.S.A. Species Location Introduction date Removal/Extinction date # Animals introduced Most recent population estimate Squirrel Monkey Bartlett Estate, Ft. Lauderdale, Broward County 1940s or 1970s N/A Unknown 3 (2014) Squirrel Monkey Silver Springs State Park, Silver Springs, Marion County Approx. 1960 1970s Unknown Extinct Squirrel Monkey Masterpiece Gardens, Lake Wales, Polk County Approx. 1960s Mid 1980s Unknown Extinct Squirrel Monkey Naples, Collier County Approx. 1960s 2010 Unknown Extinct Squirrel Monkey Florida Atlantic University, Boca Raton, Palm Beach County 1970 Late 1970s 65 Extinct Vervet Monkey Dania Beach, Broward County 1950s N/A Unknown 35 (2015) Rhesus Macaque Silver Springs State Park, Silver Springs, Marion County 1930s 1948 N/A Approx. 12 175 (2015) Rhesus Macaque Titusville, Brevard County 1976 Early 1990s Unknown Extinct Rhesus Macaque Key Lois & Raccoon Key, Monroe County 1973 & 1978 1999 2000 1350+ Extinct

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41 Figure 2 1. Adult Squirrel Monkey ( Saimiri sciureus ) in Ft. Lauderdale, Florida Photo by Steve Johnson Figure 2 2. One juvenile and two adult Vervet Monkeys ( Chlorocebus sabaeus ) in Dania Beach, Florida Photo by C. Jane Anderson.

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42 Figure 2 3. One infant and two female adult Rhesus Macaques ( Macaca mulatta ) in Silver Springs, Florida Photo by C. Jane Anderson.

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43 Figure 2 4. Approximate locations of introduced non human primate populations in Florida, U.S.A.

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44 CHAPTER 3 PREDATION OF ARTIFICIAL NESTS BY INTRODUCED RHESUS MACAQUES ( M acaca M ulatta ) IN FLORIDA, U.S.A. Introduction Florida has had the most non native wildlife species introductions of any U.S. state (Hardin 2007) Prevention, management, and mitigation of invasive species in the state cost over $500 million annually (Beck et al. 2008) Florida is especially vulnerable to non native species introductions due to its large numbers of tourists, several major ports of entry, thriving exotic pet trade, peninsular geography, and subtropical environment. Three species of non human primates have established populations in Flori da: the squirrel monkey ( Saimiri sp. ), the vervet monkey ( Chlorocebus sabaeus ), and the rhesus macaque ( Macaca mulatta ). Among the non human primates introduced in Florida, rhesus macaques may pose the greatest threat to native wildlife species and natural resources. Ranging from Afghanistan to the west, the Pacific coast of China to the east, and central India and Laos to t he south, they are believed to have the widest native range of any non human primate (Southwick et al. 1996). They have proven capable of adapting to an extensive diversity of habitats ranging in elevation from sea level to 4000m. They are both arboreal an d terrestrial, and they are particularly adept at thriving in human settlements (Fooden 2000) They are primarily herbivorous, but supplement their diet with small vertebrates and invertebrates, honeycombs, and bird eggs (Fooden 2000) 1 In introduced habita ts rhesus macaques have increased bacteria loads in water bodies 1 Reprinted with permission from Anderson, C.J., M.E. Hostetler, K E. Sieving, and S. A. Johnson. 2016. Predation of artificial nests by introduced rhesus macaques ( Macaca mulatta ) in Florida, USA. Biological Invasions 18:2783 2789

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45 (Klopchin 2008), destroyed mangrove trees leading to shoreline erosion (Kruer 1996), caused millions of dollars in crop destruction (USDA 2008), and threatened native wildlife populations ( US FWS 2011) When introduced into non native habitats, macaque species (genus Macaca ) have proven to be aggressive nest predators Crab eating macaques ( Macaca fascicularis ) were introduced on the island of Mauritius in the 1500s; nest predation by this popu lation may have contributed to the extinction of the dodo ( Raphus cucullatus ; Hume and Walters 2012) and continues to be a substantial threat to breeding birds on the island (Safford 2011) Japanese macaques ( Macaca fuscata ) introduced in Texas were found to depredate artificial ground nests (Feild et al. 1997) Managers of St. tailed macaques ( Macaca silenus ) in 1991 (Dierenfeld and Mccann 1999) and subsequently removed the animals after they proved to be aggre ssive towards humans and voracious predators of native bird eggs and hatchlings (R. Hayes, pers. comm. ). Perhaps the most significant threat of introduced macaques to breeding birds in the U.S. is the introduced population of rhesus macaques in Desecheo Is land National Wildlife Refuge, located off the western coast of Puerto Rico. The island historically provided home to tens of thousands of breeding seabirds. In the early 1900s, the introduction of non native rodents began a decline of seabird nesting. Rhe sus macaques were introduced in 1966, and nest predation by the macaques was severe enough to halt all seabird reproduction on the island within a few years. Managers have subsequently implemented an intense macaque removal program on the island (USFWS 201 1).

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46 Rhesus macaques were introduced into what is today Silver Springs State Park (SSSP), central Florida, in the 1930s in an effort to increase tourism. The initial introduction included approximately six animals, and an additional six animals were release d in 1948 (Wolfe and Peters 1987) A 1968 study estimated the population had grown to 78 individuals spread between two groups (Maples et al. 1976) By the 1980s the macaque population reached nearly 400 animals (Wolfe and Peters 1987). Several trapping ef forts between 1984 and 2012 resulted in a removal of approximately 1,000 rhesus macaques from SSSP (Wolfe and Peters 1987; Florida DEP Public Records 2013). This removal effort was halted after extensive public controversy. In f all 2015 there were approxim ately 190 macaques in SSSP (C.J. Anderson, pers. observation ), however there are no current management strategies or population control measures. The cessation of macaque removal has the potential to lead to significant population growth. It is not current ly understood how this population growth could impact native species. Wolfe and Peters (1987) reported the rhesus macaques in SSSP did not consume bird eggs when presented with them. This appeared to contradict evidence collected from other introduced rhes us macaque populations ( USFWS 2011) In an effort to reconcile this apparent contradiction, we conducted a study to determine whether rhesus macaques in SSSP would consume bird eggs placed in artificial nests in the natural environment. Methods Study Site The area which is now SSSP became a tourist attraction in the 1870s (DEP 2015). The 4,685 acre park was purchased by the state of Florida in 1985 (DEP 2014).

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47 It is an IUCN Category V Protected Landscape/Seascape (Hubbard and Judd 2013). The Silver River fl ows entirely within SSSP before flowing into the Ocklawaha River. During fiscal year 2012 2013 the park attracted approximately 243,080 visitors, contributed approximately $11 million in direct economic input and provided 179 jobs to the area (DEP 2014). T he park contains twenty one unique natural communities and is home to eighteen endemic and ten endangered plant species (Hubbard and Judd 2013). This diversity of natural communities provides critical habitat for resident and migratory birds, including eig ht imperiled species ( DEP 2014 ). Study Design We conducted a study in areas of SSSP known to be occupied by the macaques from April through July 2014, which corresponded with the breeding period of passerine birds in the habitat. We conducted our study in four replicate study sites, one in the estimated range of each of four macaque groups (Figure 2 1). Whil e home ranges of each macaque group were unknown, we selected locations where each respective group had been observed at least two times (B. Gottschalk, pers. comm. ). Groups were distinguished by location, group size, age/sex composition, and by individual s with unique physical characteristics. Within each study site we marked a 240m transect every 10m using flagging tape, for a total of 25 points per transect (100 total in the study). We placed one nest to the right or left of each marked point at a minimu m distance of 5m from the transect; this was done so the flagging tape would not become a visual cue for macaques to locate nests. Each nest was baited with two quail eggs and one clay egg; clay eggs were used because tooth marks left in the clay can assis t with identifying nest predators. We used commercially produced, open cupped artificial (wicker) nests, and placed them in shrubs or trees 0.5m 2m from the ground to

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48 represent typical nesting sites of several common shrub nesting species in the study si te (e.g., Northern Cardinal ( Cardinalis cardinalis ), Eastern Towhee ( Pipilo erythrophthalmus ), Northern Mockingbird ( Mimus polyglottos ), Brown Thrasher ( Toxostoma rufum ), White Eyed Vireo ( Vireo griseus ), Prairie Warbler ( Setophaga discolor ), Red Winged Bl ackbird ( Agelaius phoeniceus ); C. Anderson, pers. observation ). To minimize human scent, we handled the nests with nitrile or latex gloves, left them outdoors for a minimum of three days prior to placing them in the field (Sieving and Willson 1998), and li ned the nests with natural materials from the field site to hide the wicker. Nests were left in the field for 12 days, the average incubation period of Northern Cardinals, with an adjacent camera trap set to record all motion. We checked the nests and came ras one time after 5 8 days to ensure the cameras were functioning with sufficient battery and memory capacity and to remove depredated nests. Nests were counted as depredated if eggs were removed, scratched, or had tooth marks. We use a combination of th e camera trap data and field signs to attempt to identify the predator of each depredated nest. Nests depredated by macaques typically had all three eggs removed and were removed from the vegetation, and typically the predation event was clear on the camer a footage. No predation event was captured on video by a predator other than macaques, but nests consumed by non macaque predators were identified through field signs not indicative of macaques; for example, only one egg would be removed or tooth/scratch m arks on the eggs were too small to have been attributed to a macaque. Nests were characterized as an unknown predator

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49 if the field signs were potentially indicative of a macaque, but the camera was not activated by the predation event. Analyses We used th e camera trap data to determine the day each nest was depredated by a macaque. We used the Mayfield estimator in Program MARK (Dinsmore and Dinsmore 2007) to estimate the day of nest depredation for those consumed by non macaque predators and to calculate Daily Survival Rate (DSR) for all nests. We compared DSR between nests depredated by macaques and other predators. To determine the relative abundance of macaques between sites, we used the timestamps recorded by the camera traps to determine the minimum number of days the macaques were present in each study site during the respective study period. We conducted a logistic regression to determine if the proportion of nests depredated by macaques in each of the four sites was correlated with the number of da ys macaques were present in the respective site ( = 0.05; Agresti 2002) using R (version 3.0). Results Of the one hundred nests, two were lost to inclement weather and excluded from the study. Of the remaining ninety eight, twenty one nests were depredate d by macaques (Figure 2 2), nine nests by other predators, and five nests were consumed but the predator could not be identified with certainty (Table 2 1). Nest consumed by macaques had a higher DSR (0.97) than those consumed by other predators (0.68; Tab le 2 2), indicating nests depredated by predators other than macaques were destroyed earlier in the study than those destroyed by macaques. We determined the proportion of nests depredated by macaques was positively correlated to macaque relative abundance ( P <0.001), indicating nest mortality rate by macaques increased

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50 with macaque relative abundance (Table 2 3). The odds ratio was 1.75 (95% C.I. 1.40 2.19), which suggested for each day macaques were present in a site, the likelihood of a nest being depr edated by macaques nearly doubled. Post hoc observations indicated a single macaque group may have visited two of the research sites, indicating we may have sampled three macaque groups rather than four; however, because no group specific analyses were con ducted (e.g., impacts of macaque group age ratio on nest predation rates), this did not impact our results. Discussion Artificial nests lack the parental care and protection of natural nests, they cannot fully mimic native passerine nests in size, smell, o r placement, and predation rates may be influenced by researcher presence (Major and Kendal 1996) Therefore, the results of this study do not suggest rhesus macaques in SSSP are consuming 21% of native shrub nesting bird nests, nor does it confirm they ar e capable of locating native passerine nests. However, it does confirm rhesus macaques in SSSP will consume eggs when they locate them in the natural habitat. We believe this merits concern regarding the potential impact of this introduced population to na tive breeding birds. Rhesus macaques are believed to be opportunistic rather than intentional or specialized nest predators, which aligns with our observation that they were less efficient at locating nests than other nest predators in SSSP. As generalist omnivores with broad diets and opportunistic diet choices (Fooden 2000), macaques are very likely to encounter and depredate natural bird nests at rates correlated with macaque density or relative abundance. This suggests that in areas where macaque popul ations achieve higher abundance, bird nests will be at proportionately greater risk of macaque predation. However, the net indirect effects of macaques on nest predation rates via

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51 interactions with other nest predators (e.g., squirrels, raccoons, etc.) in SSSP is unknown. Macaque effects on nest loss could (a) be additive (if abundance of other predators are unaffected by macaques), (b) be compensatory (if macaques replace other predators in determining nest losses), or (c) result in decreased overall nest mortality (if macaques reduce other predator abundance and eliminate their portion of nest loss). Given that the non macaque nest predators attacked nests more quickly than macaques (Table 2 2), and that Site 4 had the highest macaque relative abundance an d the highest nest mortality, we suggest that additive predation by macaques may be more likely than compensatory predation effects on bird nest success. Without knowing the effect of macaques on native nest predators, we hypothesize that areas with high m acaque abundance could experience relatively high nest mortality rates because of their generalist foraging and likelihood that their predation pressure on native nests could be additive. Replicating this and similar studies both in and outside of macaque ranges would provide additional valuable information for determining the direct and indirect effects of macaques on native species, which would be useful for managers. We provide the first confirmation that introduced rhesus macaques are potential nest predators in the continental U.S. Compared to island bird species (e.g., those in Desecheo Island National Wildlife Refuge) that do suffer from introduced macaque nest pre dation, it is unlikely the common breeding birds in SSSP are experiencing negative population responses to nest mortality at the current rhesus macaque population size and density. Many continental bird communities evolved sympatrically with very diverse n est predators, and in turn they exhibit generalized nest defense strategies (e.g., nest guarding, inconspicuous nest placement, multiple nestings per season); similar nest

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52 defense strategies are often lacking in island birds that evolved nave of native ne st predators (Humphrey et al. 1987), making them vulnerable to introduced predators. However, our results clearly show that bird eggs are on the macaque menu in SSSP and that macaque nest depredation may well add to native rates of nest loss. For natural a reas with sensitive bird species nesting sympatrically with introduced macaques, especially in areas that are frequented by macaques, the inclusion of nest contents in macaque diets should be of concern to managers. Specific to SSSP, our findings are conce rning because the population of rhesus macaques in the park is below carrying capacity and likely rebounding from its current estimated 190 animals upwards, in the direction of the previous high of nearly 400 animals (Wolfe and Peters 1987). It is possible the current population size of rhesus macaques in SSSP is causing minimal environmental impacts, however if allowed to grow uncontrolled, the predatory effects of this population on native birds could become problematic. Primates pose a unique challenge i n invasive species ecology. At least nine macaque species have successfully established populations outside of their native range (Wolfe and Peters 1987; Feild et al. 1997; Dierenfeld and McCann 1999; Lowe et al. 2000; Long 2003) Crab eating macaques are (Lowe et al. 2000). Macaques introduced throughout the world pose various environmental, economic, and human health threats. However, macaques hold cultural and religious significance in ma ny cultures (Radhakrishna et al. 2013) and even in introduced ranges can increase tourism and subsequent revenue for natural areas (Wolfe and Peters 1987) Managers of macaque introduced habitats must

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53 carefully balance ecological considerations with public perceptions of these charismatic, yet potentially destructive animals.

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54 Table 3 1. Nest Mortality by Study Site Total # nests used # nests depredated by macaques # nests depredated by other predators # nests depredated by unknown predator # days macaques present in study site Study Site 1 25 2 0 1 2 Study Site 2 25 3 1 1 1 Study Site 3 25 1 3 1 2 Study Site 4 23* 15 5 2 7 TOTAL 98 21 9 5 *Twenty five nests were placed on the transect, however 2 were lost to inclement weather Table 3 2 Daily Survival Rate of Depredated Nests by Predator DSR Standard error Lower confidence interval Upper confidence interval Nests Depredated by Macaques 0.973 0.006 0.959 0.982 Nests Depredated by Other Predators 0.682 0.105 0.452 0.848 Nested Depredated by Unknown Predators 0.802 0.085 0.586 0.921 Table 3 3. Logistic Regression Predicting Proportion of Nests Depredated by Macaques by Macaque Abundance Coefficient Standard Error P value Intercept 3.3478 0.5732 <0.001 Macaque Abundance 0.5596 0.1141 <0.001

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55 Figure 3 1. Locations of the four study sites in SSSP Figure 3 2. Image captured by a camera trap of a rhesus macaque consuming a quail egg from an artificial nest Photo by C. Jane Anderson.

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56 CHAPTER 4 WINTER HOME RANGE AND HABITAT SELECTION OF AN INTRODUCED POP U LATION OF RHESUS MACAQUES ( M acaca M ulatta ) IN FLORIDA, U.S.A. Introduction Ranging throughout Asia and northern Africa, macaques (genus Macaca ) have the largest geographic range of any genus of non human primates (Thierry et al. 2004; Fleagle 2013) The diversity of environmental and climatic conditions to which many macaque species are able to adapt has allowed humans to successfully introduce at least nine macaque species into novel habitats since the 16 th century (Wolfe and Peters 1987; Feild et al. 1997; Dierenfeld and McCann 1999; Lowe et al. 2000; Long 2003) At least four macaque species have been documented to cause environmental and econ omic degradation in introduced habitats (Feild et al. 1997; Lowe et al. 2000; Long 2003) Among these, rhesus macaques ( Macaca mulatta ) arguably represent one of the most successful and destructive invasive primate species in the world. Native throughout southern and eastern Asia, rhesus macaques have the largest geographic range of any non human primate species (Southwick et al. 1996) They are capable of adapting to a diversity of environmental conditions including subtropical, temperate and subalpine ha bitats, ranging in elevation from sea level to 4,000m (Fooden 2000) They are both arboreal and terrestrial. Although primarily herbivorous, they supplement their diet with invertebrates, small vertebrates, honeycombs, and bird eggs (Fooden 2000). Their ad aptable nature allows them to thrive and cause extensive environmental and economic degradation in introduced habitats. Documented examples include crop destruction (Engeman et al. 2010) bacterial contamination of water (Klopchin et al. 2008) destruction of mangroves leading to shoreline erosion (Kruer

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57 1996) and decreased island bird populations due to egg and chick predation (Evans 1989) Although the natural habitat of rhesus macaques consists of forests and edge habitats, they are noted synanthropes t hat thrive in human dominated habitats (Richard et al. 1989) In human dominated landscapes rhesus macaques receive provisional feeding through hand outs from humans, trash pilfering, and crop raiding. Human provisioned food is often higher in caloric valu e, available more readily and in larger relative abundance than natural foods, therefore requiring less energy expenditure to attain than natural foods. Consequently, provisioned primate populations demonstrate earlier sexual maturity, longer survival, rap id population growth, larger densities (Sengupta et al. 2015) and decreased foraging of natural foods (Jaman and Huffman 2013), compared to non provisioned populations A review of rhesus macaque natural history found average home ranges in provisioned pop ulations are one third the size (0.65 km 2 ) of non or minimally provisioned populations (1.96km 2 ; Fooden 2000). Similarly, population densities were over five times greater in non forested habitats (i.e., areas with provisional feeding; 201.1/km 2 ) compared to forested habitats (i.e., areas with no or limited provisional feeding; 37.2/km 2 ; Fooden 2000) Approximately six rhesus macaques were introduced into what is today Silver Springs State Park (SSSP), central Florida, USA, in the mid 1930s in an effort to increase tourism, and approximately six additional animals were added around 1948 (Wolfe and Peters 1987) The 1968 population was estimated to be 78 individuals between two groups (Maples et al. 1976) By the late 1970s the population had spread to the f orests adjacent to SSSP (Montague et al. 1994), and by the mid 1980s the

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58 population within SSSP reached nearly 400 individuals (Wolfe & Peters 1987; Wolfe 2002) From 1984 to 2012, approximately 1,000 rhesus macaques from SSSP and approximately 130 additio nal macaques from adjacent lands were trapped and removed. The majority of these animals were sold into biomedical research. This caused extensive controversy among local citizens and animal rights activists, and as a result trapping efforts stopped in 201 2. The population was estimated to include 118 animals in s pring 2013 (Riley and Wade 2016) and over 175 animals in f all 2015 (Anderson, personal observation ). Understanding habitat use of invasive species is important for evaluating potential impacts on natural resources and developing management strategies (Adams et al. 2014) In this study we determined the winter home range and habitat selection of a group of rhesus macaques in SSSP. Although feeding wildlife is prohibited in SSSP, the rhesus macaques are provisionally fed by tourists in boats along the Silver River (Riley and Wade 2016) Because provisional feeding from humans can alter rhesus macaque behavior and population dynamics (Jaman and Huffman 2013; Sengupta et al. 2015) we also evaluated whe ther this may be influencing winter home range and habitat use. Methods Study Site SSSP was purchased by the state of Florida in 1985 (Florida Department of Environmental Protection 2014). The park is situated around the Silver River, a spring fed river which flows east into the Ocklawaha River (Figure 4 1). The 4,685 acre park contains a diversity of natural communities that provide habitat for eighteen endemic and ten endangered plant species (Hubbard and Judd 2013) and at least ten imperiled

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59 wildlife s pecies (Florida Department of Environmental Protection 2014 ; Florida Fish and Wildlife Conservation Commission 2016) Animal Capture and Collar Placement We selected a site within SSSP in which our target macaque group had been previously observed (Anderso n et al. 2016) To habituate the macaques to the trap site, we pre baited the site daily using corn and fresh produce beginning mid November 2014. The study was conducted in winter when natural food is less abundant to enhance the effect of baiting (Joll y et al. 2003) I n early December o nce the macaques were traveling to the site more than four days per week we added eight 48 inch box live traps (Tomahawk Live Trap Company, Hazelhurst, WI) These were wired open to prevent unintentional capture and to habituate the animals. Traps were wrapped with plastic mesh to avoid bait stealing (Jolly et al. 2003). Our aim was to trap and collar an adult female. Female macaques remain with their natal groups their entire lives. The movements of a single female, the refore, act as a proxy for the entire group (Izumiyama et al. 2003) We modified the traps so they could be triggered by a line, rather than a treadle, to prevent capture of non target animals. The traps were controlled from camouflaged blinds built from l arge, fiberglass water tanks (developed by W. Hyde, USGS, 2014). On the morning of December 18, 2014 we captured two adult female macaques. We selected the larger for inclusion in the study and released the smaller female. We immobilized the animal with a n intramuscular injection of ketamine (4mg/kg) and dexmedetomidine (40 ug/kg) using a blow dart to fit the animal with a GSM radio collar (Followit, Lindesberg, Sweden). The collar weighed 210g, or 3.2% of the weight of the animal (6.5kg), congruent with t he Guidelines of the American Society of Mammalogists

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60 (Sikes 2016) Rhesus macaques are diurnal and roost in trees at night (Fooden 2000) Thus, we scheduled the collar to record coordinates every two hours from 06:30 to 20:30 to evaluate daily movement. A n additional point was taken at 23:30 to determine A study duration of one year was initially planned. However, on February 2 nd the collar was observed to be causing neck abrasions. The following day a release signal was sent for the collar to drop off. We repeated release signals February 4 th 8 th Because the collar did not immediately fall off, we attempted to re trap the anim al from February 5 th 8 th The collar dropped off without manual intervention on February 9 th and the collar was retrieved using VHF signal. The animal was observed to recover rapidly from the neck abrasions after collar removal. Our initial study design included collaring a female from each of the five of the macaque groups in SSSP. A fter the abrasions caused by the collar lead to negative publicity on social media, however, we were targeted by animal rights activists and chose to discontinue the study. Data Analysis Although t he collar was on the animal from December 18 February 9 th o nly the data from December 20 th February 4 th were included in the analyses of home range and habitat selection. The dates before and after these were excluded because we were providing bait for the animals, potentially biasing group movements (Hill 1999; Fooden 2000; Jaman and Huffman 2013) Home range was determined using the fixed kernel density (KD) method using a 95% probability distribution and a least squares cross v alidation smoothing parameter (Worton 1989) This method uses clusters of the datapoints on a grid surface to identify areas most frequently used. Home range was also calculated using the minimum convex polygon (MCP) method including 95% of

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61 observed locati ons (Harris et al. 1990) to allow comparison with previous rhesus macaque studies (Klegarth 2015) ; this method creates a polygon around the datapoints where no angle is less than 180 (Harris et al 1990) Home range analyses were conducted using the adehab itatHR package in R Version 3.3.1 (Calenge 2006) Habitats types were defined using the Florida Natural Areas Inventory guidelines (1990) and consolidated using Hubbard and Judd (2013) Habitat selection was determined as the proportion of time spent in ea ch habitat type within the home range (Erickson et al. 2001; McDonald et al. 2005) Boater use of the Silver River is higher on weekends than weekdays (Florida Department of Environmental Protection 2014; Riley and Wade 2016), suggesting the macaques are more likely to receive provisional feeding from boaters on weekends than weekdays. To determine if the macaques were more likely to be in close proximity to the Silver River on weekends than weekdays, we calculated the distance of each recorded point withi n the home range to the Silver River using ArcGIS. We then conducted a means comparison (t weekdays than weekends R esults Home range was estimated to be 0.65 km 2 using the 95% KD estimate and 1.26km 2 using the MCP estimate. Of the 381 fixes included within the home range, 83% were within floodplain swamp, 16.5% were in hydric hammock, and a single point in an urban area (Figure 4 1). On weekends, 91% of coordinate s within the home range were within floodplain swamp and 9% were within hydric hammock. On weekdays, 80% of coordinates were within floodplain swamp and 20% were within hydric hammock. The average distance of coordinates to the Silver River was smaller on weekends (75.68m;

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62 n=113) than weekdays (92.29m; n=268; t statistic = 1.6279; p = .05). The rhesus macaques crossed the river on eleven days; only two of these days had multiple fixes on the south side of the river. All nightly roosting fixes were on the north side of the river. Discussion than the MCP estimate a nd appears to be a better representation of their true home range (Figure 4 1). The Silver River likely influences the shape of the home range (see below), and consequently the MCP method artificially inflates the home range estimate. Rhesus macaque home r ange and habitat selection can vary by season (Neville 1968; Lindburg 1977; Fooden 2000) T hus, it is possible the results of this study do not The rhesus macaques in SSSP predominately selected floodpl ain swamp, suggesting this habitat is beneficial to them in winter months. This may be due to the biotic and abiotic natural resources available in this habitat. Proximity to fresh water (Lindburg 1977; Dong Ming et al. 2012) and increased canopy cover (Do ng Ming et al. 2012) are among natural resources selected by rhesus macaques in their native range. The floodplain swamp offers the rhesus macaques constant access to freshwater, as well as greater foraging diversity and canopy cover than the habitats the rhesus macaques did not utilize (e.g., sandhill, scrub, flatwoods; FNAI 1990) Further, the composition of the floodplain swamp vegetation may offer preferred food resources or important fallback food resources during winter (Marshall et al. 2009) Riley a nd Wade (2016) found ash ( Fraxinus sp. ), sedges ( Carex spp. Rhyncospera sp. ) and grasses ( Panicum spp. ) were the most frequently consumed plant species by the SSSP rhesus

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63 macaques in the winter and early spring, and Wolfe and Peters (1987) noted cabbage p alm ( Sabal palmetto ) was frequently consumed by this population. Both of these studies were conducted in the floodplain swamp and therefore do not reflect the foraging habits of the rhesus macaques in their entire home range. Most of the frequently foraged plant species reported in these studies (ash, sedges, sabal palm) are more available in floodplain swamp than in hydric hammock or the habitat types the macaques did not use (FNAI 1990) If these species are preferentially selected by the rhesus macaques, use of the floodplain swamp may be influenced by selection for these species. Home ranges of rhesus macaque groups overlap, but groups typically have core areas unoccupied by other groups (Makwana 1978; Ciani 1986) When groups interact there is often ant agonistic behavior and groups display a hierarchical order (Ciani 1986; Fooden 2000) The group in this study predominantly occupied the northern shore of the Silver River near the springhead and only occasionally crossed to the southern shore. Further, ex cursions to the southern shore never exceeded three fixes, and all roosting locations were on the northern shore. A second group of rhesus macaques occupied the area along the southern shore and was observed to display dominant behaviors over the study gro up (Anderson, personal observation ). It is therefore possible the home range and habitat use of the study group was influenced by other rhesus macaque groups in the park. Unfortunately, because we had to discontinue our study, we were unable to acquire mov ement data for other groups and unable to quantify intergroup movement behavior.

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64 Rhesus macaque home range and habitat selection in SSSP appears to be influenced by supplemental feeding by boaters on the Silver River. On weekends the rhesus macaques spent a greater proportion of time in floodplain swamp, and remained in closer proximity to the Silver River, as compared to weekdays. Further the SSSP winter home range of rhesus macaques, as estimated by MCP, was larger than regularly provisioned rhesus macaqu e groups (e.g., Teas et al. 1980; Jiang et al. 1991) and smaller than home ranges of non provisioned rhesus macaque groups (e.g., Neville 1968; Makwana 1978; Seth & Seth 1983) Riley and Wade (2016) reported 13% of observed foraging events along the Silver River were human provisioned and 87% were of natural foods. Further research is merited to determine whether provisional feeding is decreasing rhesus macaque consumption of natural resources, thereby potentially reducing resource competition with native species. Conversely, future research should investigate whether feeding is causing the rhesus macaque population to grow faster or reach greater density than it would without supplemental food resources. Our results indicate native floral and faunal specie s in floodplain swamp are at a greater risk of impact from the introduced rhesus macaque population in SSSP during winter than those in other habitats. Winter food resources are likely limited in the floodplain swamp for herbivores, as this habitat type co nsists of primarily deciduous tree species (FNAI 1990) and demonstrates decreased seed abundance in winter (Titus 1991) Foraging of vegetation by the rhesus macaques (Wolfe and Peters 1987; Riley and Wade 2016) may alter forest composition or reduce alrea dy limited winter food resources for native herbivores (Charles and Dukes 2007; Lockwood et al. 2007)

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65 Native species may also be vulnerable to interference competition (e.g., aggressive interactions) from rhesus macaques (Anderson, personal observation ; P eters 1983) Because habitat selection can vary seasonally (Neville 1968; Lindburg 1977; Fooden 2000) it is possible the floodplain swamp is used disproportionally more frequently by rhesus macaques in the winter than other seasons. Anderson et al. (2016) found rhesus macaques in SSSP consumed bird eggs placed in artificial nests in their habitat, indicating they may consume natural nests when they encounter them. Thus, if the macaques select floodplain swamp during the bird breeding season, populations of birds that nest in this habitat ( including seven species listed as imperiled in the state of Florida ) (Florida Fish and Wildlife Conservation Commission 2016) may be vulnerable to rhesus macaque occupancy. Management of invasive species is difficult and controversial, particularly when the species is charismatic (Verbrugge et al. 2013) Our study indicates rhesus macaques are potentially influenced by human provisioning. Management efforts should, therefore, be directed towards educating boaters in SSSP t o prevent feeding. Our experience receiving threats from animal rights activists illustrates how contentious research and management of introduced primates can be. The negative environmental and economic impacts of other introduced macaque populations (Evans 1989; Kruer 1996; Klopchin et al. 2008; Engeman et al. 2010), however, highlight the importance of continued research and management of this population. Future research and management of introduced primate species, including the rhesus macaques of S SSP, should include extensive public education, transparency of research objectives and methods, and careful consideration of local opinions and sentiments

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66 Figure 4 1. Winter home range estimates of a group of rhesus macaques in Silver Springs State Pa rk, Florida, U.S.A., using minimum convex polygon and kernel density methods

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67 CHAPTER 5 POPULATION ESTIMATE AND MANAGEMENT OPTIONS OF INTRODUCED RHESUS MACAQUES IN SILVER SPRINGS STATE PARK, FLORIDA, USA Introduction Humans have intentionally or uni ntentionally relocated non human primates (hereafter: primates) to novel habitats for at least five centuries (Long 2003). At least 10 primate species have been introduced in the United States over the past century. Chimpanzees ( Pan troglodytes ; Wilson and Elicker 1976) lion tailed macaques ( Macaca silenus ; Mowery et al. 1997) and three species of lemurs ( Lemur sp. ; Yabsley et al. 2007) were intentionally introduced on islands off the Atlantic coast of Georgia for research or conservation; all have since been removed except ring tailed lemurs ( Lemur catta personal observation ). Japanese macaques ( Macaca fuscata ) were introduced on a private ranch in Texas in the 1970s (Fedigan 1991, Paterson 1996) ; this population was subsequently moved to a fenced enclosure (Born Free USA Primate Sanctuary 2016) after extensive population growth and threats to environmental resources (Feild et al. 1997) Since the 1930s, populations of squirrel monkeys ( Saimiri sp .), vervet monkeys ( Chlorocebus sabaeus ) and rhesus macaques ( Macaca mulatta ) have successfully established in Florida (Anderson et al., University of Florida, In Review ). Rhesus macaques are the most common primate species used in biomedical research (Han nibal et al. 2016) The majority were historically imported from India, but in 1978 the country banned primate export (Malik 1989, Crockett et al. 1996) Consequently, U.S. based biomedical companies sought inexpensive methods of developing breeding coloni es, by establishing free ranging rhesus macaque colonies on islands (Crockett et al. 1996, Johnsen et al. 2012) In the 1960s and 1970s rhesus

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68 macaques and patas monkeys ( Erythrocebus patas ) were introduced to the islands of Cueva and Guayacn, Puerto Rico but later escaped to the mainland of Puerto Rico. In 2008 the invasive populations of these animals were estimated to cause over $1 million annually in crop losses and management expenses (Engeman et al. 2010), and they have been subsequently controlled with an extensive culling program (Lpez Ortiz 2016) In 1979, over 1,400 rhesus macaques were introduced to Morgan Island, South Carolina (Taub and Mehlman 1989, Klopchin et al. 2008) ; tidal creeks surrounding the island were subsequently found to have el evated levels of fecal coliform and Escherichia coli as a consequnce of the macaques (Klopchin et al. 2008) Between 1973 1978 over 1,300 rhesus macaques were introduced to Key Lois and Raccoon Key, in the Florida Keys (Lehman et al. 1994, Johnson and Kaps alis 1998) These animals destroyed red mangroves ( Rhizophora mangle ), leading to shoreline erosion (Kruer 1996) and likely decreased bird populations (Hoffman 1996, Enge et al. 2002) ; the animals were subsequently removed after extensive legal proceedings (Anderson et al., University of Florida, In Review ). In 1966, Rhesus macaques were introduced to what is now Desecheo National Wildlife Refuge, Puerto Rico, a critical nesting habitat for tens of thousands of seabirds, to study behavioral adaptations of p rimates; while seabird nesting had begun declining after the introduction of black rats in the early 1900s, the island was fully abandoned as a nesting habitat by 1970 due to the added predation of eggs and chicks by the rhesus macaques. This population of rhesus macaques has since been controlled through trapping and removal (Evans 1989) The ability of rhesus macaques to thrive in novel environments is likely due to their plasticity in habitat requirements. This species has the largest native range of any

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69 non human primate (Southwick et al. 1996) Their native and invaded habitats range from sea level to altitudes of 4000m (Fooden 2000) They are both arboreal and terrestrial. Rhesus macaques are largely herbivorous but supplement their diet with small ver tebrates, invertebrates, eggs, and honeycomb (Fooden 2000). They live in groups with an alpha male, multiple females and their offspring, and subordinate males. Females remain with their natal groups their entire lives; most males leave their natal group a fter reaching sexual maturity, then live independently or in bachelor groups until they join a new group (Maestripieri and Hoffman 2012) Rhesus macaques are synanthropes, thriving in human dominated landscapes (Richard et al. 1989) and selecting for dist urbed habitats (Goldstein and Richard 1989) In urban and suburban areas in their native range, rhesus macaques receive provisional food from human feeding, raiding trash bins, and crop raiding. Provisional food provided from humans is usually calorically rich, more abundant, reliable, and requires less energy expense when compared to natural foods (Sengupta et al. 2015) Consequently, average group size of provisioned rhesus macaque populations is larger (76.9) than non provisioned groups (32.3). Similarly population densities are five times larger on average in human dominated habitats (201.1/km 2 ) than forested habitats (0.65 km 2 ; Fooden 2000) Increased population growth and density in human dominated habitats has necessitated rhesus macaque population control in both their native and introduced ranges, including: trapping and removal (Southwick et al. 1980, Malik et al. 1984) culling via eutha nasia (Wang and Quan 1986, Saraswat et al. 2015, Lpez Ortiz 2016) and sterilization (Wellem 2014, Ocean Park Foundation 2016) Variation in

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70 anthropogenic sentiment towards this species complicates and influences management strategies. Human macaque confl ict (e.g., crop raiding, aggression) has led many to regard this species as a pest. Conversely, many of the Hindu faith (the predominant faith in India) regard macaques as sacred, and feeding and protecting them is an important tradition to many practicing this faith (Pirta et al. 1997, Radhakrishna et al. 2013, Saraswat et al. 2015) Consequently, rhesus macaque populations surrounding Hindu temples are among the largest and densest in the world (Fooden 2000, Radhakrishna et al. 2013) History of Rhesus Macaques in Central Florida Rhesus macaques were introduced in the 1930s into Silver Springs, a tourist attraction on the Silver River in Central Florida, to increase tourism. The original introduction included approximately six individuals released on an island in the Silver River. Rhesus macaques are proficient swimmers, which allowed the animals to swim across the Silver River and establish on the river banks. Approximately six additional macaques were released around 1948 (Wolfe and Peters 1987, Hammond 1989) By 1968 the population was estimated at 78 individuals between two groups (Maples et al. 1976) and by the late 1970s had spread to expanded to natural areas beyond the original introduction location at Silver Springs (Montague et al. 1994) By 197 9 the macaque population in this area had grown to more than 150 individuals (Sarris 1980) and had reached almost 400 animals by 1984 (Wolfe and Peters 1987, Wolfe 2002). Based on these estimates of abundance, the 1968 1984 annual rate of population grow th was approximately 11%.

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71 Rhesus Macaque Management in Central Florida This population density caused an increase in negative human macaque interactions (e.g., bites and scratches). Managers were concerned about the potential for the macaques to spread th e zoonotic Herpes B Virus to humans; although transmission to humans is extremely rare, it can be fatal ( Huff and Barry 2003 Jones Engel et al. 2006; see Discussion). At the same time, natural resource managers were becoming concerned the macaque populati on may have negative impacts on a variety of native species, including depredation of bird nests (Montague et al. 1994) which instigated management efforts (M. Summers, personal communication ). In 1984, approximately 225 animals were trapped and removed f rom Silver Springs and sold to a biomedical research supply company. These removals triggered extensive negative feedback from the public, which caused resource managers to eliminate the trapping program (Wolfe 2002) The lack of public support led to a ce ssation of most state implemented trapping. In the following years, approximately 60 rhesus macaques were removed without state permission, and others were captured and sent to a zoological park (Wolfe and Peters 1987). While removal records were not maint ained during this period, Wolfe (2002) estimated 500 macaques were removed from 1984 1993. In the late 1980s, 13 female macaques were sterilized by hysterectomy in an effort to decrease population growth (Wolfe 2002) From 1998 2012, an estimated 832 rhesu s macaques were trapped and removed from SSSP and adjacent lands, approximately 630 of which were from SSSP (Florida Public Records 2013). These animals were also sold into the biomedical research industry. Again, this incited controversy and protest from animal rights groups, leading to termination of the removal effort. There have been no management efforts since 2012. Riley and Wade (2016) estimated the s pring 2013

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72 population prior to the end of birthing season to be 118 individuals (111 among 4 grou ps and 7 peripheral males). While past trapping and removal efforts were controversial (Wolfe and Peters 1987), they may have controlled the population of rhesus macaques in SSSP. The aim of this study was to inform management plans with the goal of mainta ining or reducing this population. To achieve this, we estimated the f all 2015 population size of rhesus macaques in Silver Springs State Park (SSSP). Additionally, we used age structured matrix models to estimate future population growth and how long it w ill take for the population to reach the size previously deemed problematic by managers (N = 400). We then modeled future abundance using culling and sterilization, management practices that have been used to control native and other introduced rhesus maca que populations. S tudy A rea Silver Springs State Park was purchased by the State of Florida in 1985. The 19km2 park is situated along the Silver River, a spring fed river which flows east into the Ocklawaha River (Figure 5 1). The park contains 21 natural communities (FNAI 2016) and provides habitat for 18 endemic and 10 endangered plant species (Hubbard and Judd 2013). In 2012 2013 the park attracted 243,080 visitors, provided 179 jobs, and was estimated to contribute $11 million in directed economic input (FL DEP 2014). The park is managed by the Florida Department of Environmental Protection. Wildlife management throughout the state of Florida is under the direction of the Florida Fish and Wildlife Conservation Commission.

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73 M ethods Data were collected on r hesus macaque population size from September 27 November 14, 2015. This study was conducted in SSSP with permission from the Florida Department of Environmental Protection (Permit Number 01281413). Our research protocol was approved by the University of Florida Animal Ethics Committee (IACUC Protocol Number 201308022). Population Estimate We identified the number of rhesus macaque groups by size, age/sex composition, location, and individuals with unique physical features (Hasan et al. 2013, Jaman and Huf fman 2013). The two groups of rhesus macaques nearest the headspring of the Silver River, and therefore in closest proximity to humans, were habituated to human presence on land (hereafter: Groups I & II). This allowed us to conduct point count censuses fo r these two groups (Seth and Seth 1983, Imam and Ahmad 2013, Jaman and Huffman 2013) using bait spread in open, grassy areas. Individuals were counted in four age/sex classes: adult males, adult females, subadults, and infants (Southwick et al. 1980, Johns on et al. 1988). Counts with these groups were repeated until two observers independently counted the same number of individuals at least three times. The three groups in the central and eastern portions of SSSP were not habituated to humans on land, prohi biting us from conducting point counts (hereafter: Groups III V). Thus, we used camera traps to estimate the size of these groups. Camera traps provide an efficient mechanism for studying unhabituated, terrestrial primates (Gerber et al. 2014, Li et al. 2015) We placed 11 camera trap stations in the floodplain swamp, five on the north bank and six on the south bank, with approximately

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74 1km between each station (Figure 5 1). The floodplain swamp was selected because the rhesus macaques select this habitat in winter months (Anderson et al., University of Florida, unpublished data ). Each camera trap station had four camera traps facing in opposing directions, with a minimum of 15m between each. Corn was placed in front of each camera daily to attract the rhesus macaques. Four of the stations could only be reached by ATV or boat, so automatic corn dispensers were placed in these sites to ensure daily baiting. We used the came ra trap data to count the number of individuals in the four aforementioned age and sex classes during each minute the rhesus macaques were present in the station. Double counting of individuals was prevented by the synchronized time stamps of the camera tr aps and by the distance between the camera traps. Although rhesus macaque groups forage collectively, this method did not allow us to observe every individual in the group simultaneously. Minimum group size was estimated as the largest number of individual s simultaneously observed within each respective age/sex class. Sex could not be distinguished in the infant or subadult age classes using the cameras and was assumed as a 1:1 ratio (Berman 1988, Bercovitch et al. 2000) Groups I & II frequented the camera trap stations. We used our census data for these groups to determine detection probability (Gerber et al. 2014, Mackenzie et al. 2016) of the camera trap method. Detection probability was calculated as the proportion of the number of individuals in each a ge/sex class observed from the camera trap data divided by the known number of individuals in each age/sex class from the census data (Rowcliffe et al. 2008; Table 5 1) The detection probability was then used to estimate the number of individuals in Group s III V based on minimum group size observed from

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75 the camera trap data (Tables 5 2 & 5 3). We calculated the proportion of individuals in each age class. Fertility (F x ) was calculated as the ratio of infants to adult females (Wolfe and Peters 1987, Hernnd ez Pacheco et al. 2013, Tian et al. 2013) Model Design We used age structured matrix population models to estimate future population growth of rhesus macaques in SSSP using discrete, annual time steps (Caswell 2001, Hernndez Pacheco et al. 2013, Hernand ez Pacheco et al. 2016) These models incorporate fertility (F x ) and predicted survivorship (P x ) by age class to project future population size. Because female rhesus macaques are promiscuous (Wolfe 2002, Maestripieri and Hoffman 2012) reproductive succes s is not limited by adult males (Rawlins and Kessler 1986; Hernndez Pacheco et al. 2013) We, therefore, created the matrix models based only on females within the population (Hernndez Pacheco et al. 2013) Infants were classified as those < 1 year old; we assumed equal sex ratio of infants (Berman 1988, Bercovitch et al. 2000) and that infant survival did not vary by sex (Hoffman et al. 2010) Subadults were categorized as one and two year olds; we therefore assumed one half of surviving subadults would become adults each year (Malik et al. 1984; Figure 5 2) Although three year old rhesus macaque s are sometimes considered subadults (Southwick and Siddiqi 1977, Johnson et al. 1988) the average age at first birth for female rhesus macaques is four (Drickh amer 1974, Tian et al. 2013) Our 2015 population estimate was conducted during the Fall, which is the breeding period of rhesus macaques in SSSP (Hammond 1989), and our population models were conducted with annual timespans with respecitve estimates in th e Fall Because most females are sexually mature during the breeding season of their third

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76 year (Bercovitch and Harvey 2004) adult females were considered to be those age three and older. The initial population size within the models was based on our f all 2015 population estimate, with the number of infants and subadults estimated as one half of the total number of individuals in these age classes (because we assumed equal sex ratio in these age classes), as well as the total estimated number of adult fema les. We used one half of the predicted fertility (F x ) to estimate the fertility of adult females producing female infants (F f ; Hernndez Pacheco et al. 2013, Tian et al. 2013 ). Because the population was known to be well below potential carrying capacity, the models excluded density dependence (Crockett et al. 1996, Hernandez Pacheco et al. 2016) All models were conducted using R (version 3.2.5, www.r project.org, accessed 15 June 2016). Model Parameterization Because survival by age class is unknown in SSSP, we used survivorship rates from published studies of other rhesus macaque populations in our models (Crockett et al. 1996) Two of the studies derived age specific survivorship from growing populations, Her nandez Pacheco et al. (2013) and Jiang et al. (1998), and two from stable populations, Johnson et al. (1988) and Southwick et al. (1980; Table 5 4) We used estimated survival rates from the four studies to predict how long it will take the SSSP population to reach 400 individuals, the population size deemed problematic by managers in the mid 1980s (Figure 5 3). We estimated the total number of individuals in the population at each time based on the predicted number of females (from the models) and the pred icted female:male ratio. Because infants and subadults were assumed to have a 1:1 sex ratio, our values from the female only models were doubled. Post hoc observations suggested the adult male to female ratio was 1:2.3 (see Results).

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77 Therefore, for every f emale projected to be in the population at a given time, we estimated there would be 0.43 males. Population size was not predicted beyond 400 because the carrying capacity of rhesus macaques in SSSP is unknown (see Discussion). We compared the models using survivorship rates from other populations to determine which best represented past population growth based on the population 11%). We selected the survivorship rates from this study for further analyses. Sensitivity and e lasticity of this model were evaluated to Caswell 1978, de Kroon et al. 2000, van de Kerk 2009) We used the survivorship rates from this study to model future population s ize under four management scenarios: 1) culling 50% of subadults and adults; 2) culling 80% of subadults and adults; 3) sterilizing 50% of sexually mature females (age three and older); and 4) sterilizing 80% of sexually mature females (age three and older ). Because the efficacy of management strategies can be influenced by the timing and frequency of implementation (Abrams 2009, Wells et al. 2016) we modeled the four management scenarios implemented at four timescales: annually, bi annually, every five ye ars, and every 10 years. R esults Population Estimate There were a total of 81 macaques between Groups I and II (Table 5 1). From the camera traps we were able to detect 60 macaques between these two groups. Detection probability varied by age and sex cla ss: 83% for adult males and females, 54% for subadults, and 100% for infants (Table 5 1). Using the camera traps we observed 78 individuals between the Groups III V (Table 5 2). After accounting for

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78 detection bias, we estimated there were 95 individuals ac ross these three groups (Table 5 3). Overall, we estimated 176 individuals among the five groups (Table 5 3). Fertility, the proportion of infants to adult females, was estimated to be 78%. Population Modeling the four reported studies (Figure 5 3). The models projected population growth using survival rates reported by Hernandez (19 0.936). The annual growth rate using the survivorship rates from Hernandez Pacheco et a l. (2013) was the closest to previous population growth in SSSP and was, therefore, selected for further analyses. Sensitivity and elasticity analyses indicated adult survivorship (S a o ther parameter (Figure 5 4). Using the survivorship rates reported by Hernandez Pacheco et al. (2013), the female population was projected to reach extinction by 2019 if 80% of subadults and adults were culled annually and by 2024 if 50% of subadults and a dults were culled annually (Figure 5 5). The population was projected to reach extinction by 2022 if 80% of the animals were culled bi annually and by 2032 if 50% of the population was culled bi annually (Figure 5 5). No other culling models reached extinc tion by 2035, although the population was estimated to near extinction in 2031 if 80% of adults females were culled every 5 years (Figure 5 5). Sterilizing adult females was never projected to lead to extinction. Sterilizing 50% or 80% of adult females an nually decreased the population size to less than a third of

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79 the current size by 2035. Bi annual sterilization of 80% of adult females yielded similar results to annual sterilization of 50% of adult females. Sterilizing 80% of female adults every five year s was projected to stabilize the population. Sterilizing 50% of adult females less frequently than every other year was projected to allow continued population growth; similarly, sterilizing 80% of adult females every 10 years projected population growth ( Figure 5 5). D iscussion Compared to native and other introduced rhesus macaque populations, the current population size of rhesus macaques in SSSP is quite small (Fooden 2000). The estimated age and sex composition of the rhesus macaque population in SSSP was similar to native populations. The ratio of adult male to female rhesus macaques was 1:2.3, similar to numbers reported in native populations in India (Makwana 1978, Seth and Seth 1983) and previous reports of the SSSP population (Wolfe and Peters 1987 ) Sexually immature individuals comprised 59% of the population, consistent with native populations undergoing population growth (Southwick et al. 1980) The fertility rate of 78% was similar to rhesus macaque populations in tropical and subtropical clima tes (Southwick et al. 1996) as well as a previously reported fertility rate in SSSP by Wolfe and Peters (1987; 81%) Reported annual growth rates for increasing rhesus macaque populations range from 3.8% to 26.9% (Fooden 2000) In ideal ecological settings, rhesus macaque populations can double in four years (Malik et al. 1984) Wolfe and Peters (1987) reported a single group of rhesus macaques in SSSP grew from 22 individuals in 1976 to 100 individuals in 1986, an approximatel y 16.5% annual growth rate; this group was receiving daily provisions of food, and the authors suggested other macaque groups in

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80 the park were likely growing at a slower rate (Wolfe and Peters 1987) Growth rates of rhesus macaque populations are often inf luenced by anthropogenic forces; for example, extensive population growth can occur after the cessation of trapping (Malik et al. 1984) This may indicate the 2015 population growth rate was closer to our estimate based on the survival rates of Jiang et al (1998) and that our management models based on the survivorship rates of Hernandez Pacheco et al. (2013) are conservative. Unfortunately, the annual growth rate between 2013 and 2015 cannot be determined by comparing this study with the 2013 estimate by Riley and Wade (2016; 111 individuals between four groups), as the previous study was conducted prior to the end of the 2013 birthing season and this study was conducted after the conclusion of the 2015 birthing season. However, the difference in populatio ns estimates between these studies suggests th e SSSP population is growing. Rhesus macaque populations demonstrate density dependent biosocial mechanisms of population control. Southwick et al. (1980) suggest this is typically through reduced natality and /or increased mortality among subadults and adults. The SSSP rhesus macaque population was assumed to be growing in 2015, as indicated by a population size less than half of the population size of the mid 1980s (N However, it is nearly impossible t o project the potential carrying capacity of this population, or the point at which the population will begin demonstrating density dependent population regulating mechanisms. The rhesus macaques of SSSP appear to select floodplain swamp (Anderson, unpubli shed data ), however it is unknown what other habitat types in SSSP (e.g., sandhill, mesic flatwoods) can also support them. Thus, population growth may be limited by resource availability. Conversely, the rhesus

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81 macaques are regularly fed by tourists on bo ats in the Silver River (Figure 5 6; Riley and Wade 2016) which may cause their population to grow larger or denser than it would without provisional feeding (Fooden 2000, Sengupta et al. 2015) The provisional feeding of rhesus macaques in SSSP likely e xacerbates the potential public health threats of this population. Macaques can be aggressive towards humans, and incidents of dangerous human macaque interactions are amplified by feeding macaques (Sha et al. 2009) The population of rhesus macaques in SS SP has tested seropositive for the zoonotic Herpes B virus (Montague et al. 1994) Macaques are the natural host of this virus, and infected macaques demonstrate few or no physical symptoms (Huff and Barry 2003) Seroprevalence of Herpes B virus is 10 80% in wild populations of rhesus macaques and can reach 100% in captive populations (Jones Engel et al. 2006) The virus is transmitted through exposure to bodily fluids (e.g., saliva, urine) of an infected individual. Between macaques this is through social activity (e.g., grooming, sexually activity, fights; Burgos Rodriguez 2011) Humans are most often exposed by a bite or scratch from an infected animal (Burgos Rodriguez 2011, Lee et al. 2015) Like other herpesviruses, the virus can only be spread when th e infected individual is shedding the virus (Burgos Rodriguez 2011) Despite countless exposures of humans to macaques infected with Herpes B around the world, there have been no confirmed reports of a human expressing symptoms of the virus after exposure from a macaque in the wild (Engel et al. 2002, Jones Engel et al. 2006, Burgos Rodriguez 2011) There have, however, been 50 documented cases of humans contracting the virus from macaques in captive settings, nearly half of which (n = 21) were fatal (CDC 2 016) The reason for the apparent absence of transmission from

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82 macaques in the wild but fatality of transmission from captive macaques is unknown. It is possible there are multiple strains of the virus (some more pathenogenic to humans than others). Wild m acaques may shed the virus less frequently than captive macaques (decreasing frequency of transmission potential). It is also possible there have been non reported or misdiagnosed cases of human infection (Burgos Rodriguez 2011) Because the threat of Herp es B virus to humans is poorly understood, it is difficult to ascertain the degree to which it should be considered in managing the population of rhesus macaques in SSSP. Managers of rhesus macaque occupied habitats should ensure visitors are aware of the virus and how to protect themselves. The SSSP rhesus macaque population may impact native flora and fauna species. Interactions with native species may include exploitation competition (e.g., limiting availability of foraging resources) or interference com petition (e.g., aggressive behavior of rhesus macaques towards native species). Anderson et al. (2016) found the rhesus macaques in SSSP consumed quail eggs placed in artificial nests in their habitat, suggesting they may depredate nests of native breeding birds. Additional research is needed to evaluate current or potential impacts of this population on the native natural resources of SSSP. This study and historic population estimates indicate this population is capable of extensive growth, which may lead to expansion into other areas. The adjacent population of rhesus macaques along the Ocklawaha River and into Ocala National Forest appears to be an expansion of the SSSP population (Montague et al. 1994) From 2011 2016, there were at least 38 sightings o f rhesus macaques outside of SSSP in Florida (EddMapS 2016) It is unknown if these animals were emigrants from the

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83 SSSP population or came from other sources (e.g., escaped pets). The models in this study do not account for environmental, demographic, or genetic stochasticity, and consequently cannot precisely predict future population sizes (van de Kerk 2009) Rather, our projections can be used by managers to compare tradeoffs between different management strategies as a guideline for decision making. Ou r findings indicate population management is necessary to prevent continued population growth and expansion. The current management plan for SSSP includes the removal of non native species (FL DEP 2014) While managers of this park have previously attempt ed population control of introduced rhesus macaques through trapping and removal, the lack of public support has repeatedly terminated this practice. Managers of SSSP need to carefully evaluate the trade offs between eradication and maintenance management (Simberloff 2003, Simberloff et al. 2005) of rhesus macaques in SSSP, and the related ecological, economic, and public perception consequences. Our models indicate the most effective management action to reduce population size is through culling. Prior to the 1978 ban of primate exports, the rhesus macaque population in India dwindled in response to the trapping and removal of animals for sale into the research industry (Malik et al. 1984, Malik 1989) however, the population rebounded quickly after the tr apping ban (Southwick et al. 1986, Malik 1989) The introduced population of Japanese macaques in Texas was trapped and moved into a fenced enclosure (Born Free USA Primate Sanctuary 2016) which eliminated a free ranging and problematic population (Feild e t al. 1997) Our sensitivity and elasticity analyses indicated subadult survivorship was far less influential on population growth

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84 rates than adult survivorship. This is important to consider in any culling program because trapping is typically most succes sful among subadults due to trap naivety (Hernandez Pacheco et al. 2016) Our results indicate a culling program would need to remove adult macaques to hinder or halt population growth. For adult animals, culling via euthanasia may be necessary if traps a re avoided to ensure the removal program is effective. A culling program was implemented for the invasive rhesus macaque and patas monkey populations in Puerto Rico in 2009, and by 2016 both populations were nearly eradicated (R. Lpez Ortiz personal commu nication ). We cannot state with certainty the population of rhesus macaques in SSSP can be fully eradicated. Our models assumed the population was closed to immigration. If managers successfully removed the current population of rhesus macaques from SSSP, it is possible the SSSP population could be restored via immigration from surrounding rhesus macaque populations (e.g., EddMapS 2016) The current size and distribution of rhesus macaques outside of SSSP is unknown, and the likelihood of immigration canno t be predicted. Maintaining, or reducing, the current population size of rhesus macaques in SSSP without fully eliminating it may prevent rhesus macaques from surrounding areas from immigrating into SSSP, either through aggression or lack of resource avail ability due to the occupant rhesus macaques (Ciani 1986, Fooden 2000). This could potentially afford researchers and managers additional time to evaluate these surrounding populations and determine effective management strategies at the metapopulation leve l. Maintaining or reducing the current population size of introduced rhesus macaques in SSSP could be accomplished through sterilization. At least three options

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85 are available for female contraception. Females in SSSP were previously sterilized via hystere ctomy (Hammond 1989); while effective, this invasive procedure cannot be conducted in the field and requires a monitored recovery period. A sterilization program began in Hong Kong in 1998, representing the first large scale macaque sterilization program ( Wellem 2014) Females were initially injected with SprayVac TM an immuno contraceptive vaccine which has been demonstrated to provide at least three years of contraceptive effects in mammals (Fraker et al. 2002) While this method demonstrated initial success in field trials (Wong and Chow 2004) it had limited long term effectiveness with the macaque population in Hong Kong (K. Martelli, personal communication ). In 2009, managers in Hong Kong began using an endo scopic tubectomy procedure to sterilize adult females and vasectomize males (Wellem 2014, OPCF 2016) These strategies can be performed in the field and do not require recovery periods in captivity (K. Martelli, personal communication ). This program reduce d the fertility rate from over 60% in 2009 to less than 30% in 2015 (OPCF 2016). This program is implemented annually and aims to sterilize 80% of adult females (OPCF 2016). M anagement I mplications Management of charismatic invasive species is controversia l (Verbrugge et al. 2013) but public support can be critical to the success of environmental management programs (Jacobson 2009) Culling the rhesus macaques be less expensive than sterilization (Wellem 2014) and our models suggest it would reduce the pop ulation more quickly and more effectively than sterilization. If managers prioritize complete removal of the population, trapping and removal or euthanasia should be effective W e do not however, recommend resuming the practice of selling trapped rhesus m acaques from

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86 SSSP into biomedical research. Previous managers, trappers, and researchers of the rhesus macaque population in SSSP have received violent and legal threats from animal rights activists (Anderson, personal observation ). A population control pr ogram that lacks public support would not only create negative public perceptions, but could be dangerous for personnel Further, the history of public involvement with this population suggests a management protocol lacking public support is not sustainabl e. A sterilization program with extensive prior public outreach and education is more likely to receive public support than culling (Barr et al. 2002, Wellem 2014) and would offer reverence to the public sentiment and cultural significance of this species (Radhakrishna et al. 2013) Sterilization is an effective method of reducing macaque populations (Wellem 2014, OPCF 2016) and appears viable for population reduction based on our models The brief previous sterilization effort of this population in the lat e 1980s (Wolfe and Peters 1987, Hammond 1989) did not incite the same public controversy as previous trapping and removal efforts. A 2012 online petition calling for a sterilization program in lieu of a trapping program received nearly 2,000 signatures (Change.org 2016), demonstrating support from bo th the public and animal rights activists. If sterilization is to be implemented in SSSP, we suggest use of the in field tubal ligation method used by managers in Hong Kong (OPCF 2016). This would be more effective than SprayVac TM cheaper and involve red uced recovery time than hysterectomy. The synanthropic nature of rhesus macaques has led to overpopulation in human dominated landscapes in their native range (Fooden 2000, Wellem 2014) and the generalist habitat and diet requirements of this species has allowed it to become

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87 invasive throughout its introduced range (Evans 1989, Klopchin et al. 2008, Engeman et al. 2010) The population of rhesus macaques in SSSP provides a unique opportunity to manage a relatively small population in a novel environmental and cultural setting. Management of this population could provide important insights for rhesus macaque population management throughout the world.

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88 Table 5 1. Number of rhesus macaques observed in two habituated gr oups at Silver Springs State Park by census and camera trapping Adult Males Adult Females Subadults Infants Census Observed via camera traps Detection Probability Census Observed via camera traps Detection Probability Census Observed via camera traps Detection Probability Census Observed via camera traps Detection Probability Group I 6 4 0.67 13 10 0.77 18 9 0.5 12 12 1 Group II 2 2 1 10 9 0.9 14 8 0.57 6 6 1 Average Detection Probability 0.83 0.83 0.54 1 Table 5 2. Minimum number of animals observed via camera traps and estimated total number of animals using observed age specific detection probability of three unhabituated groups of rhes us macaques at Silver Springs State Park Adult Males Adult Females Subadults Infants Observed via camera traps Estimated via detection probability Observed via camera traps Estimated via detection probability Observed via camera traps Estimated via detection probability Observed via camera traps Estimated via detection probability Group 3 5 6 8 9 6 9 7 7 Group 4 5 6 11 13 14 21 10 10 Group 5 2 2 4 5 2 3 4 4 TOTAL 12 14 23 27 22 33 21 21

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89 Table 5 3. Estimated total number of rhesus macaques in Silver Springs State Park, using census values for two habituated groups and estimated values based on detection probability for three unhabituated groups Adult Males Adult Females Subadults Infants TOTAL Grou p 1 6 13 18 12 49 Group 2 2 10 14 6 32 Group 3* 6 9 9 7 31 Group 4* 6 13 21 10 50 Group 5* 2 5 3 4 15 Total 22 50 65 39 176 Estimated using detection probability Table 5 4. Age specific annual survival rates from other rhesus macaque populations Study Infant Survival Rate Subadult Survival Rate Adult Survival Rate Jiang et al. 1998 1 99% 99% 92.1% Hernandez Pacheco et al. 2013 1 88.1% 97.05% 88.3% Southwick et al. 1980 2 78.5% 83% 74.2% Johnson et al. 1988 3 84% 84% 77% 1 Study reported age specific survivorship. Subadult survivorship was the average reported for yearlings and two year olds. Adult survivorship was the average of all individuals age 3 and older 2 Study reported survivorship rates for subadults as age 1 2 months 48months and adults as age 48 months and older. In this study, the subadult survivorship rate was used for 1 2 year olds 3 Study reported survivorship for infants, juveniles, and adults, but did not specify age classification for juveniles

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90 Figure 5 1. Locations of camera trap stations in Silver Springs State Park, Florida

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91 Figure 5 2. Life cycle diagram and corresponding population matrix for rhesus macaques in Silver Springs State Park. In both the life cycle diagram and the matrix, P x represents the survivorship of each respective age class (P x = infant survivorship, P sa = subadult su rvivorship, P a = adult survivorship), and F x represents fertility. The solid arrows represent transition between age classes and are labeled with the survival probability for each transition. The dashed arrow represents fertility as a function of adult fe male survivorship. Subadults were categorized as yearlings and two year olds and assumed to have equal survivorship; thus, half of subadults were assumed to remain within the age class each year, and half were assumed to become adults.

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92 Figure 5 3. Projected population growth of rhesus macaques in Silver Springs State Park using reported survival rates from other rhesus macaque populations. Population size was not modeled beyond 400 individuals, as potential carrying capacity beyond this is unknown. 0 50 100 150 200 250 300 350 400 450 Jiang et al. 1998 Hernandez-Pacheco et al. 2013 Johnson et al. 1988 Southwick et al. 1980

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93 Figure 5 4. Sensitivity and elasticity measurements of infant survival (S i ), subadult survival (S sa ), adult survival (S a ), and fertility (F) of the introduced population of rhesus macaques in Silver Springs State Park, Florida.

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94 Figure 5 5. Projected female rhesus macaque population size in Silver Springs State Park, using survivorship rates reported in Hernandez Pacheco et al. (2013), under four management scenarios culling 50% of subadult and adult females, culling 80% of su badult and adult females, sterilizing 50% of adult females (age 3 and older), and sterilizing 80% of adult females (age 3 and older) and implemented at four levels of frequency annually, biannually, every five years, and every 10 years. The point at wh ich the female population (N f ) reaches 234 individuals is noted, as this is where total population (N) reaches 400, and carrying capacity beyond this is unknown.

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95

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96 Figure 5 6. Woman inciting an aggressive display from an adult female rhesus macaque ( Macaca mulatta ) by attempting to hand feed it in Silver Springs State Park, Florida Photo by C. Jane Anderson.

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97 CHAPTER 6 P ULATION S Macaques and Modern Conservation The human popula tion size increased seven times over the past century, and is projected to reach nearly 9 billion by the year 2050 (Meffe et al. 2006) This rapidly increasing population is causing irrevocable, and sometimes catastrophic, alterations to the natural world (Steffen et al. 2007) In turn, wildlife populations and biodiversity are under threat (Wilcove et al. 1998) As the human population is growing, it is also urbanizing. Expanding cities cause populations of synanthropes species that thrive in human domin ated areas to grow to problematic and sometimes dangerous level s (Sala et al. 2000; McKinney 2002) Further, as global travel and trade have increased, the number of introductions of species into novel habitats has increased (Lockwood et al. 2007) Growi ng cities are causing native species to become pests, and by moving species to new environments, humans also cause them to become invasive. Rhesus macaques ( Macaca mulatta ) represent dual conservation problems extensive population growth in human domina ted systems, and ability to thrive in novel (Richard et al. 1989) In their native range, rhesus macaque populations are rapid ly growing in synchrony with growing human populations. Population management of rhesus macaques varies across cultures and landscapes, and this variation is largely related to variation in human sentiments towards this species. An estimate from the mid 19 80s suggested 10,000 rhesus macaques were culled annually in China (Wang and Quan 1986) Populations are believed to be controlled in Laos and Vietnam through hunting (IUCN

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98 2016) Hong Kong began an extensive sterilization program in 2009, which has reduce d the population and decreased the fertility rate by half (Wellem 2014; OPCF 2016) and export for the biomedical field. This practice was banned in 1978, largely in rever Consequently the rhesus macaque population quickly rose, and in recent years has been observed to be fragmenting as the animals are drawn towards human dominated habitats (Molur et al 2003) In response to the growing and problematic population size, Himachal Pradesh, a state in northern India, reinstated rhesus macaque culling in 2016; this decision has been met with substantial controversy and public protest (Choudharyl 2016) Like most invasive species, the actions of a few ill advised humans have made rhesus macaque management a necessity in the United States. Over 1,000 rhesus macaques have been culled in Puerto Rico (Lpez Ortiz 2016) after the destruction of crops in southw estern Puerto Rico (Engeman et al. 2010) and extensive depredation of native bird eggs and chicks on Desecheo Island National Wildlife Refuge (Evans 1989) The destruction of red mangroves on two islands in the Florida Keys (Kruer 1996) led to years of lit igation and a mandatory removal of the animals (Chapter 2). Of the 10 species of non human primates that have been successfully introduced by humans into the United States, rhesus macaques have unquestionably been the most successful and problematic. Wildl ife Management in Florida Florida has had more wildlife introductions than any other U.S. state (Hardin 2007) Prevention, mitigation, and management of these species cost an estimated

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99 $500 million annually (Beck et al. 2013) The Florida Fish and Wildlife Conservation Commission (FWC) is charged with the management of wildlife species statewide. This includes monitoring native species, restoring imperiled populations, and researching and attempting to manage introduced species. There have been more than 50 0 fish and wildlife species introduced into Florida (FWC 2016a) including an estimated 17 mammals (FWC 2016b) FWC and land managers must determine how to efficiently allocate limited resources between conserving native species and controlling introduced species. Developing realistic and sustainable wildlife management strategies is difficult. Managers of wildlife population are often frustrated that management decisions cannot be made solely within the context of wildlife biology, but must also incorporat e economic limitations and sociopolitical considerations (Bath 1998) Controversial wildlife management programs designed to protect environmental resources can fail when lacking public support (Jacobson 2009) This is not to suggest public perception shou ld be the only, or even the primary, consideration when developing wildlife management strategies, but rather to emphasize that public opinion cannot, and should not, be disregarded. Introduced Non Human Primate Populations My objectives of my dissertation research were to determine the history and current status of non human primate populations in Florida (Chapter 2), to evaluate the potential impacts of rhesus macaques in SSSP (Chapters 3 4), and to estimate the current size and future growth of the population size of rhesus macaques in SSSP (Chapter 5). My aim was to use the results of this research to provide insight for developing management strategies for non human primate populations locally and

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100 throughout Florida. Given the dispari ties in invasion success, potential threats, and public involvement, I believe management strategies must be tailored to each respective introduced non human primate species in Florida. Despite having the most introduced populations in Florida (n = 5), sq uirrel monkeys have thus far had limited success in surviving in the state. Should future populations of squirrel monkeys develop, they will certainly merit research and monitoring. However, I suggest the remaining three individuals in Ft. Lauderdale do no t pose a significant enough threat to environmental or anthropogenic resources to merit management intervention. The vervet monkey population of Dania Beach is reported to have established in the 1950s (Williams 2015). A comparison of the mid 1990s popula tion size reported by Hyler (1995) and 2015 population size reported by Williams (2015) suggests this population has demonstrated little change in the past 20 years. There may be potential environmental and human health threats from this population F or ex ample, vervet monkeys depredate nests in urban habitats (Patterson et al. 2016) and can carry zoonotic pathogens. They can also be aggressive towards humans; a motorist in Dania Beach was reportedly charged by several of the vervet monkeys after unintentio nally hitting one with their car (Nolin 2013). However, there is extensive public support for this population, including residents who make a daily habit of feeding these monkeys (D. Williams, personal communication ). When FWC previously considered impleme nting a removal strategy with this population, local officials responded by considering a local ordinance protecting the monkeys (J. Ketterlin Eckels, personal communication ). Additional research is merited to further assess the behaviors and potential hum an

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101 health threats of this population. However, given the current small population size, lack of demonstrated impact, and extensive public support, I argue aggre ssive management is presently unnecessary. Among the nine introduced populations of non human primates in Florida (Chapter 2), the population of rhesus macaques in Silver Springs State Park (SSSP) is the oldest, largest, and fastest growing. In this study, I demonstrated this population may be problematic for native breeding birds (Anderson et al. 2016; Chapter 3) may compete with native species utilizing Floodplain Swamp for winter resources (Chapter 4), and, without management intervention, will likely double in size by 2022 (Chapter 5). I also provided models suggesting this population could be reduced and perhaps eradicated through management (Chapter 5). The historic population growth demonstrated by this population, coupled with the findings of this study, suggest management intervention is needed to prevent further population growth and relat ed impacts. The problem now lies in determining the best management strategy, which incorporates ecological, economic, and social considerations. The previous method of trapping the rhesus macaques in SSSP and selling them to the biomedical research indust ry has repeatedly been unsuccessful due to lack of public support. Further, researchers, managers, and trappers of this population have received violent threats from animal rights extremists. My experience receiving threats after radio collaring a rhesus m acaque (Chapter 4) gave me first hand experience with how frustrating and scary this can be. A management strategy lacking public support may prove dangerous for practitioners, and is likely to be unsustainable.

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102 The macaque population in Hong Kong has been successfully reduced through sterilization (Wellem 2014), and research has found this is a favorable option among the public. Further, both animal rights activists and the general public in Florida have demonstrated approval of sterilizing the SSSP rhesus macaque population (Change.org 2016). This strategy is by no means a silver bullet. It would likely be more expensive than alternative methods (Wellem 2014) and our models suggest it would be unlikely to fully eradicate the population (Chapter 5). Further it could potentially set a problematic precedent by causing members of the public to expect sterilization as a solution for all overpopulations and invasive species. Management of charismatic invasive species is extremely difficult (Verbrugge et al. 201 3) Government agencies are responsible for managing wildlife populations, which means making necessary decisions to protect native species. As humans, we management stra tegy for the rhesus macaque population in SSSP is no easy feat. However, it has important implications for management of rhesus macaque populations around the world. I encourage managers to continue researching this population, to facilitate communication with other macaque managers around the world, and to be extremely transparent to the public in the decision making process.

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103 LIST OF REFERENCES Abee, C. 1985. Medical care and management of the squirrel monkey. Pages 447 488 in L. Rosenblum and C. Coe, editors. Handbook of squirrel monkey research. Plenum Press, New York, NY, USA. Abrams, P. A. 2009. When does greater mortality increase population size? The long history and diverse mechanisms underlying the hydra effect. Ecology Letters 12:462 474. Adair, E. 1985. Thermoregulation in the squirrel monkey. Pages 219 252 in L. Rosenblum and C. Coe, editors. Handbook of squirrel monkey research. Plenum Press, New York, NY, USA. Adams, A. L., M. R. Recio, B. C. Robertson, K. J. M. Dic kinson, and Y. van Heezik. 2014. Understanding home range behaviour and resource selection of invasive common brushtail possums ( Trichosurus vulpecula ) in urban environments. Biological Invasions 16:1791 1804. Agresti, A. 2002. Logistic regression. Pages 1 65 210. Categorical data analysis. 2nd Edition. John Wiley & Sons, New Jersey, USA. Anderson, C. J., M. E. Hostetler, K. E. Sieving, and S. A. Johnson. 2016. Predation of artificial nests by introduced rhesus macaques ( Macaca mulatta ) in Florida, USA. Biol ogical Invasions 18:2783 2789. Bair, B. 1981. Masterpiece monkeys still driving Curtis bananas. Lakeland Ledger. < https://news .google.com/newspapers?nid=1346&dat=19810605&id=348sAAAAIB AJ&sjid=MPsDAAAAIBAJ&pg=1743,1700939&hl=en > Accessed 13 September 2016. Bair, B. 1983. Spider monkeys leaving like Masterpiece Gardens. Lakeland Ledger. < h ttps://news.google.com/newspapers?nid=1346&dat=19831226&id=E6lOAAAAIB AJ&sjid=afsDAAAAIBAJ&pg=2138,4090999&hl=en > Accessed 13 September 2016. Baldwin, J. 1985. The behavior of squirrel monkeys in natural environments. Pages 35 54 in L. Rosenblum and C. Coe, editors. Handbook of squirrel monkey research. Plenum Press, New York, NY, USA. Barr, J. J. F., P. W. W. Lurz, M. D. F. Shir ley, and S. P. Rushton. 2002. Evaluation of immunocontraception as a publicly acceptable form of vertebrate pest species control: The introduced grey squirrel in Britain as an example. Environmental Management 30:342 351. Bath, A. J. 1998. The role of huma n dimensions in wildlife resource research in wildlife management. Ursus 10:349 355.

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104 Beck, S., A. Clarke, L. Perez, and D. Feiber. 2013. Florida Invaders. National Park Service and Florida Fish and Widlife Conservation Commission. Bercovitch, F. B., and N. E. Harvey. 2004. Reproductive life history. Pages 61 80 in B. Thierry, M. Singh, and W. Kaumanns, editors. Macaque societies: a model for the study of social organization. Cambridge University Press, Cambridge, United Kingdom. Bercovitch, F. B., A. Widdig and P. Nrnberg. 2000. Maternal investment in rhesus macaques ( Macaca mulatta ): Reproductive costs and consequences of raising sons. Behavioral Ecology and Sociobiology 48:1 11. Berman, C. M. 1988. Maternal condition and offspring sex ratio in a group of free ranging rhesus monkeys: an eleven year study. The American Naturalist 131:307 328. Born Free Primate Sanctuary. 2016. History of the sanctuary. < http://www.bornfreeusa.org/sanctuary/ b2_history.php >. Accessed 13 September 2016. Brennan, E., J. Else, and J. Altmann. 1985. Ecology and behavior of a pest primate: vervet monkeys in a tourist lodge habitat. African Journal of Ecology 23:35 44. Brown, J., and A. Kodric Brown. 1977. Turnover rates in insular biogeography: effect of Immigration on extinction. Ecology 58:445 449. Burgos Rodriguez, A. G. 2011. Zoonotic diseases of primates. Veterinary Clinics of North America Exotic Animal Practice 14:557 575. of space and habitat use by animals. Ecological Modelling 197:516 519. Caswell, H. 1978. A general formula for the sensitivity of population growth rate to changes in life history parameters. Theorectic al Population Biology 14:215 230. Caswell, H. 2001. Matrix Population Models. Sinauer Associates, Inc., Sunderland. Massachusetts, USA. Centers for Disease Control and Prevention (CDC). 2016. B Virus (herpes B, monkey B virus, herpesvirus simiae and herpe svirus B ). < https://www.cdc.gov/herpesbvirus/index.html >. Accessed 13 September 2016. Charles, H., and J. S. Dukes. 2008. impacts of invasive species on ecosystem services. Pages 214 238 in M. M. Caldwell, G. Heldmaier, R. B. Jackson, O. L. Lange, H. A. Mooney, E. D. Schulze, and U. Sommer, editors. Biological Invasions. Springer Verlag, Berlin, Germany.

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106 Enge, K.M., B.A. Millsap, T.J. Doonan, J.A. Gore, N.J. Douglass, and G.L. Sprandel. 2002. Conservation plans for biotic regions in Florida containing multiple rare or declining wildlife taxa. Technical Report No. 20. Florida Fish and Wildlife Conservation Commission. Tallahassee, Florida. Engel, G. A., L. Jones Engel, M. A. Schillaci, K. G. Suaryana, A. Putra, A. Fuentes, and R. Henkel. 2002. Human exposure to Herpesviurs B seropositive macaques, Bali, Indo nesia. Emerging Infectious Diseases 8:789 795. Engeman, R. M., J. E. Laborde, B. U. Constantin, S. a Shwiff, P. Hall, A. Duffiney, and F. Luciano. 2010. The economic impacts to commercial farms from invasive monkeys in Puerto Rico. Crop Protection 29:401 4 05. Erickson, W. P., T. L. McDonald, K. G. Gerow, S. Howlin, and J. W. Kern. 2001. Statistical issues in resource selection studies with radio marked animals. Pages 209 245 in J. J. Millspaugh and J. M. Marzluff, editors. Radio Tracking and Animal Populat ions. Academic Press, London, United Kingdom. Evans MA (1989) Ecology and removal of introduced rhesus monkeys: Desecheo Island National Wildlife Refuge, Puerto Rico. 8:139 156. Fedigan, L. M. 1991. of the Arashiyama west macaques in Texas. Page 353 in L. M. Fedigan and P. J. Asquith, editors. The monkeys of Arashiyama: thirty five years of research in Japan and the West. State University of New York Press, New York, NY, USA. Feild, J. G., S. E. Henke, and J. G. Mccoy. 1997. Depredation on artificial ground nests by Japanese macaques: the unspoken exotic in Texas. Great Plains Wildlife Damage Control Workshop Proceedings 367. Fleagle, J. 2013. Old World Monkeys. Pages 119 150 in Primate Adaptation and Evolution. Academic Press, San Diego, California, USA. Florida Atlantic University Digital Library (FAU). 2016. A squirrel monkey gets feed, 1967. < http://fau.digital.flvc.org/islandora/object/fau%3A3078 > Accessed 11 July 2016. Florida Department of Environmental Protection (DEP). 2014. Silver Springs State Park Draft Unit Management Plan Amendment. < http://www.dep.state.fl.us/pa rks/planning/ssag/Silver_Springs_draft_management _plan_amend.pdf >. Accessed 13 September 2016. Fooden, J. 2000. Systematic review of the rhesus macaque, Macaca mulatta (Zimmermann, 1780). Field Museum of Natural History, Chicago, Illinois, USA. Forchhammer, M. C., E. Post, N. C. Stenseth, and D. M. Boertmann. 2002. Long term responses in arctic ungulate dynamics to changes in climatic and trophic processes. Population Ecology 44:113 120.

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108 Harris, S., W. J. Cresswell, P. G. Forde, W. J. Trewhella, T. Wollard, and S. Wray. 1990. Hom e range analysis using radio tracking data: a review of problems and techniques particularly as applied to the study of mammals. Mammal Review 20:97 123. Harrison, M. 1983. Patterns of range use by the green monkey, Cercopithecus sabaeus at Mt. Assirik, Senegal. Folia Primatologica 41:157 179. Hasan, K., M. A. Aziz, S. M. R. Alam, Y. Kawamoto, L. Jones R. C. Kyes, S. Akhtar, S. Begum, M. M. Feeroz, and L. Jones Engel. 2013. Population variation in group size and composition distribution of rhesus macaq ues ( Macaca mulatta ) in Bangladesh: inter population variation in group size and composition. 26:125 132. Haus, T., E. Akom, B. Agwanda, M. Hofreiter, C. Roos, and D. Zinner. 2013. Mitochondrial diversity and distribution of African green monkeys ( Chloroce bus Gray, 1870). American Journal of Primatology 75:350 360. Hayes, K. R., and S. C. Barry. 2008. Are there any consistent predictors of invasion success? Biological Invasions 10:483 506. Heckathorn, D. D. 1997. Respondent driven sampling: a new approach t o the study of hidden populations. Social Problems 44:174 199. Hernndez Pacheco, R., D. L. Delgado, R. G. Rawlins, M. J. Kessler, A. V. Ruiz Lambides, E. Maldonado, and A. M. Sabat. 2016. Managing the Cayo Santiago rhesus macaque population: the role of density. American Journal of Primatology 78:167 181. Hernndez Pacheco, R., R. G. Rawlins, M. J. Kessler, L. E. Williams, T. M. Ruiz Maldonado, J. Gonzlez Martnez, A. V. Ruiz Lambides, and A. M. Sabat. 2013. Demographic variability and density dependent dynamics of a free ranging rhesus macaque population. American Journal of Primatology 75:1152 1164. Hill, C. M. 2000. Conflict of interest between people and baboons: crop raiding in Uganda. International Journal of Primatology 21:299 315. Hill, D. A. 1999 Effects of provisioning on the social behaviour of Japanese and rhesus macaques: Implications for socioecology. Primates 40:187 98. Hoffman, C. L., J. P. Higham, A. Mas Rivera, J. E. Ayala, and D. Maestripieri. 2010. Terminal investment and senescence in rhesus macaques ( Macaca mulatta ) on Cayo Santiago. Behavioral Ecology 21:972 978. Hoffman, W. 1996. Cuban yellow warbler ( Dendroica petechia gundlachi ). Pages 375 380 in J. A. Rodgers, H. W. Kale, and H. T. Smith, editors. Rare and endangered biota of F lorida. Volume V: Birds. University of Florida Press, Gainesville, Florida, USA.

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120 BIOGRAPHICAL SKETCH Jane Anderson grew up moving around the U.S. with a family that loved to boat, fish, and hike. This allowed her to develop a love and appreciation of nature in a variety of ecosystems and landscapes. At the age of 12 she decided she wanted to become a wildlife biologist, and at 18 she had her first internship working on an osprey reintroduction project at The Wilds, the largest conservation facility in North America. She knew she had picked the right field. Jane earned her B.S. in Fisheries and Wildlife Sciences from North Carolina State University in 2007, and her M.S. in Fisheries, Wildlife and Conservation Biology from North Carolina State University in 2010. She completed her Ph.D. in Interdisciplinary Ecology from University of Florida in 2016. Between degrees Jane held professional positions wo rking for public, private, and non profit environmental organizations.