AN INTRODUCED PRIMATE SPECIES, CHLOROCEBUS SABAEUS, IN DANIA

BEACH, FLORIDA:

INVESTIGATING ORIGINS, DEMOGRAPHICS, AND ANTHROPOGENIC

IMPLICATIONS OF AN ESTABLISHED POPULATION

by

Deborah M. Williams

A Dissertation Submitted to the Faculty of

The Charles E. Schmidt College of Science

In Partial Fulfillment of the Requirements for the Degree of

Doctor of Philosophy

Florida Atlantic University

Boca Raton, FL

May 2019

Copyright 2019 by Deborah M. Williams

ii AN INTRODUCED PRIMATE SPECIES, CHLOROCEBUS SABAEUS, IN DANIA

BEACH, FLORIDA:

INVESTIGATING ORIGINS, DEMOGRAPHICS, AND ANTHROPOGENIC

IMPLICATIONS OF AN ESTABLISHED POPULATION

by

Deborah M. Williams

This dissertation was prepared under the direction of the candidate's dissertation advisor, Dr. Kate Detwiler, Department of Biological Sciences, and has been approved by all members of the supervisory committee. It was submitted to the faculty of the Charles E. Schmidt College of Science and was accepted in partial fulfillment of the requirements for the degree of Doctor of Philosophy.

SUPERVISORY COMMITTEE: ~ ~,'£-____

Colin Hughes, Ph.D. ~~ Marianne Porter, P6.D.

I Sciences

arajedini, Ph.D. Dean, Charles E. Schmidt College of Science ~__5~141'~ Khaled Sobhan, Ph.D. Interim Dean, Graduate College iii ACKNOWLEDGEMENTS

There are so many people who made this possible. It truly takes a village. A big thank you to my husband, Roy, who was my rock during this journey. He offered a shoulder to lean on, an ear to listen, and a hand to hold. Also, thank you to my son,

Blake, for tolerating the late pick-ups from school and always knew when a hug was needed. I could not have done it without them.

Thank you to my amazing field assistant, Cheryl Ruiz. She was a dedicated volunteer rain or shine. The heat, mosquitoes, and mud did not slow her down. She was committed to the project and offered insightful ideas about the research. I enjoyed our walks through the mangroves discussing monkeys, family, and life. I was fortunate to have her on my team during this study. Also, thank you to Mariah Pagan, Angel Milla, and my sister, Beth Williams, for the help with data collection and “monkey sitting” at various times during the study.

I am grateful to my advisor, Dr. Kate Detwiler, who took a chance on a rookie.

She offered much advice and support in my quest for work, life, and balance. She encouraged my research ideas and kept me centered. I learned about academia, research, and science through her guidance. I consider her a mentor and friend. I look forward to future collaborations.

Thank you to my wonderful committee who supported this project. I appreciate your valuable advice, time, and ideas to develop the research to its fullest potential.

iv This project could not have been completed without the support of the local businesses and community, the City of Dania Beach, Port Everglades, Broward County

Parks and Recreation, and Florida Fish and Wildlife Conservation Commission. I give much gratitude to the properties that allowed me the full access needed to carry out this research. They welcomed the “monkey lady” year-round and were always there to help as needed.

Thank you to my circle of friends that listened to my monkey tales. The laughs we shared are treasured. Stay tuned for more to come!

Last, but certainly not the least, I am thankful for my mom and dad’s encouragement to pursue my dream of going back to school. My heart is full knowing that my father was able to witness the start of this adventure. He enjoyed hearing my stories from the field and seeing photos of the monkeys. Although, he isn’t here to celebrate this milestone, I know he is a proud papa.

v ABSTRACT

Author: Deborah M. Williams

Title: An Introduced Primate Species, Chlorocebus Sabaeus, in Dania Beach, Florida: Investigating Origins, Demographics, and Anthropogenic Implications of an Established Population

Institution: Florida Atlantic University

Dissertation Advisor: Dr. Kate Detwiler

Degree: Doctor of Philosophy

Year: 2019

Nonnative species are reshaping global ecosystems. The success of a nonnative species hinges on both biological and cultural variables. Primates represent a minority of nonnative species but warrant research to understand ecological implications and management solutions. The Florida Fish and Wildlife Conservation Commission recognizes three species of nonnative primates in Florida that include populations of rhesus macaques (Macaca mulatta) in Marion County, squirrel monkeys (Saimiri spp.) in

Broward County, and green monkeys (Chlorocebus sabaeus) in Broward County. This study focused on the Dania Beach C. sabaeus population.

The goals of this study were to: 1) determine the geographical origins and species of the monkeys, 2) record demographics and determine population growth rate, 3) assess the public’s perception of monkeys, and 4) understand the influence of human provisioning on the population’s behavior and biology. Public surveys and direct field observations of social groups provided baseline data to show that unlike other introduced vi primates (e.g., macaques in Marion County and green monkeys in the Caribbean), the

Dania Beach monkey population has strong public support and is at risk of extinction within the next 100 years.

vii DEDICATION

To my husband, Roy, who is the most caring, supportive, and generous man I know. I am grateful to be your wife and friend.

AN INTRODUCED PRIMATE SPECIES, CHLOROCEBUS SABAEUS, IN DANIA

BEACH, FLORIDA:

INVESTIGATING ORIGINS, DEMOGRAPHICS, AND ANTHROPOGENIC

IMPLICATIONS OF AN ESTABLISHED POPULATION

List of Tables ...... xii

List of Figures ...... xiv

Introduction ...... 1

Chapter 1. The History and Genetic Origins of the Dania Beach, Florida Monkey

Population ...... 4

Introduction ...... 4

Methods...... 7

Phenotype Analysis ...... 7

Historical Data Collection...... 8

Genetic Analysis ...... 9

Sample Collection ...... 9

DNA Extraction, Amplification, and Sequencing ...... 9

Taxon Sampling ...... 10

Statistical Analysis ...... 11

Results ...... 12

Phenotype Observations...... 12

History...... 14

ix Genetics...... 17

Discussion ...... 19

Chapter 2. Demographics and Population Viability Analysis ...... 22

Introduction ...... 22

Methods...... 26

Study Site ...... 26

Demographic Data Collection...... 28

Statistical Analysis ...... 29

Results ...... 34

Group Size and Social Structure ...... 34

Births ...... 38

Mortality ...... 40

Immigration and Emigration ...... 42

Vortex Models ...... 43

Discussion ...... 45

Chapter 3. The Tolerance, Provisioning, and Wounds of the Dania Beach Monkey

Population ...... 50

Introduction ...... 50

Methods...... 55

Survey Data ...... 55

Survey Data Statistical Analysis ...... 55

Provisioning Data...... 56

Wound Data ...... 58

x Wound Data Statistical Analysis ...... 59

Results ...... 59

Survey Data ...... 59

Attitudes Towards Monkeys in Community ...... 60

Concern for Local Monkey Conservation...... 61

Provisioning the Local Monkey Population ...... 62

Provisioning Data...... 63

Wound Data ...... 66

Wound Distribution Within Age and Sex Classes ...... 66

Wound Type and Location Within Age and Sex Classes ...... 70

Discussion ...... 74

Public Perceptions, Attitudes, and Provisioning ...... 74

Wounds ...... 77

Conclusion ...... 79

Appendix ...... 82

Appendix A. Mortality Table ...... 83

References ...... 84

xi LIST OF TABLES

Table 1. Summary of Pelage Color Variation Across Species of Chlorocebus...... 8

Table 2. Vortex Model Parameters ...... 32

Table 3. Description of the Five Different Modeling Scenarios ...... 33

Table 4. Total Number of Individuals Within Each Social Group 2014–2018 ...... 35

Table 5. Vervet Social Group Sizes Across Different Locations and Studies ...... 36

Table 6. Demographics of the Social Groups 2014–2018 ...... 37

Table 7. Birth Seasonality Across Chlorocebus Populations...... 40

Table 8. Annual Birth and Death Rates for Infants Born During Study Period ...... 41

Table 9. Results from Model Scenarios (1000 Iterations) for the Dania Beach

Monkey Population ...... 44

Table 10. Provisioning Event Categories and Definitions ...... 57

Table 11. Wound Type Definitions by Severity ...... 59

Table 12. Socioeconomic Profile of the 234 Survey Participants ...... 60

Table 13. Total Provisioning Events per Site ...... 64

Table 14. Food Items Offered and Rejected During Study Period ...... 66

Table 15. Total Observed Wounds per Age/Sex Class ...... 68

Table 16. Comparative Wound Data Across Provisioned and Wild Vervet

Populations ...... 69

Table 17. Total Wound Type per Age/Sex Class ...... 70

Table 18. Expected and Observed Wound Type per Age/Sex Class ...... 71

xii Table 19. Total Wounds on Body Location per Age/Sex Class ...... 72

Table 20. Expected and Observed Distribution of Wounds on Body Parts by

Age/Sex Class ...... 72

xiii LIST OF FIGURES

Figure 1. Distribution of African Green Monkeys (Chlorocebus spp.) ...... 13

Figure 2. Dania Beach Monkeys Photographed During This Study ...... 14

Figure 3. Dania, Florida Chimp Farm Brochure, Circa 1950s ...... 17

Figure 4. Bayesian Phylogram Depicting Bayesian Posterior Probability Values

and ML Bootstrap Support Values Based on the Concatenation of the

Sex Determining Region (SRY) and the Last Intron of the Zinc Finger

(ZFY) Gene on the Y-Chromosome ...... 18

Figure 5. Bayesian Phylogram Depicting Bayesian Posterior Probability Values

and ML Bootstrap Support Values Based on the Concatenation of a

602 bp Fragment of the Hypervariable Region 1 (HV1) and the

Complete cyt b Gene from the Mitochondrial Genome ...... 19

Figure 6. West Lake Park, Dania Beach, Florida (Broward County Government,

2018) ...... 27

Figure 7. Birth Distribution and Average Rainfall per Month ...... 39

Figure 8. Kaplan-Meier Survival (in Years) of Infants Born During the Study

Period ...... 41

Figure 9. Recorded Male Emigration and Immigration Events During the Study

Period 2014–2018 ...... 43

Figure 10. Respondents in Favor of Changing Law to Protected Status for the

Monkeys per Demographic Group...... 61

xiv Figure 11. Respondents Against the Removal of the Monkeys per Demographic

Group ...... 62

Figure 12. Respondents who Would Feed the Monkeys to Survive per

Demographic Group...... 63

Figure 13. Total Provisioning Events per Category...... 64

Figure 14. Total Counts of Variation of Food Distribution Styles to the Monkeys

by Humans ...... 65

Figure 15. Observed Monthly Wounds During 12-Month Study Period (January-

December 2017) of Age/Sex Classes ...... 67

Figure 16. Distribution of Total Wounds by Body Part for Adult Males and Adult

Females ...... 73

xv INTRODUCTION

An estimated 50,000 non-native species have been introduced into the United

States (Pimentel, Zuniga, & Morrison, 2005), resulting in various ecological and economic impacts (Simberloff, Parker, & Windle, 2005). Introduced animals can be categorized on a scale from introduced to established to invasive (Colautti & MacIsaac,

2004; Lockwood, Hoopes, & Marchetti, 2013). Some introduced species are present in low densities and may not have important ecological impacts, but a few highly adaptable species have become established and widespread and cause serious ecological and economic problems (e.g., pythons in Everglades) (Dorcas et al., 2012). Only 4-19% of the non-native species introduced into the United States are considered to be potentially invasive (U.S. Congress, Office of Technology Assessment, 1993).

Florida is home to 17 species of free-ranging nonnative mammals (Florida Fish and Wildlife Conservation Commission, 2019). Of the 17 listed non-native mammals in

Florida, three are primates: Saimiri sciureus, squirrel monkey (extirpated), Chlorocebus sabaeus, green monkey (established), and Macaca mulatta, macaque (established)

(Florida Fish and Wildlife Conservation Commission, 2019). All three primate species were introduced through various zoos, research facilities, private collections, and entertainment businesses (Anderson, Hostetler, & Johnson, 2017; Hyler, 1995; Layne,

1997; Wheeler, 1990; Wolfe & Peters, 1987). The rhesus monkey, Macaca mulatta, is the most studied by anthropologists, ecologists, and biologists. Limited scientific data are

1 available on the introduced squirrel monkey (Saimiri sciureus) and vervet monkey (C. sabaeus) populations. This study focused on the introduced monkeys (C. sabaeus) in

Dania Beach, Florida. Only one scientific study was completed by William Hyler (1995) on this introduced population in 1992. Hyler recorded two social groups of monkeys in the mangroves of West Lake Park in Dania Beach, Florida. His research suggested the monkeys escaped from a failed roadside zoo in the 1950s and 1970s. He classified the monkeys as Chlorocebus aethiops or possible hybrids of Chlorocebus tantalus x

Chlorocebus pygerythrus. The monkeys were observed foraging on natural food sources

(mangroves and various invertebrates), in addition to human provided foods. Hyler stated that further research was needed to investigate origins of population and growth rate.

There are six species within the genus Chlorocebus and are widely distributed throughout Africa. In addition to Africa, green monkeys (C. sabaeus) are found in the

Caribbean as they were introduced in the 1600s during the slave trade (Dore, 2017).

Vervets (common name) are habitat generalists, limited only by the availability of water and sleeping trees (Pasternak et al., 2013; Wolfheim, 1983). Vervets are most noted for their ability to successfully exploit human environments and adapt to most environments due to their generalist biology and behavior (Saj, Sicotte, & Paterson, 1999). In many areas these monkeys are known as “pest primates” due to their food raiding activities are subject to lethal human actions (Brennan, 1985; Healy & Nijman, 2014; Patterson, Kalle,

& Downs, 2017).

The current population status, potential impacts, and species of the Dania Beach monkey population were unknown. Genetic analysis was needed to confirm the species of monkeys residing in Dania Beach, as Florida Fish and Wildlife Conservation

2 Commission (FWC) and Hyler’s (1995) research lack agreeance in taxonomy.

Interestingly, two species within Chlorocebus have been listed as either Near Threatened

(C. sabaeus) or as Vulnerable (C. djamdjamensis) by the International Union for

Conservation of Nature and Natural Resources (IUCN) (2019). Preliminary observation of the monkeys in Dania Beach suggested that the monkeys are C. sabaeus. This population could serve as an ambassador species to educate the public about conservation efforts abroad. As an introduced primate with the possibility for becoming invasive, it was imperative to determine the future trajectory of the population by recording demographic data. These data were then used in VORTEX (Population Viability Analysis software) to estimate population survival and growth. Additionally, an assessment of public opinion was completed through anonymous online surveys. Successful management plans implemented by wildlife authorities need to be reflective of public attitudes (Decker, Gavin, & Greer, 2013). The primary objectives of this study were to: 1) determine the historical origins and confirm species through genetic analysis, 2) record population size and use demographic data to determine the population viability, and 3) assess the tolerance of the monkeys by the local community. The results of this study can fill in the gaps of knowledge missing about this population and contribute to public and the FWC’s knowledge about the species. Also, the outcomes of the data can better guide any management strategies of the population if needed.

3 CHAPTER 1. THE HISTORY AND GENETIC ORIGINS OF THE DANIA BEACH,

FLORIDA MONKEY POPULATION

Introduction

Since the 1930s, at least 10 species of primates have been introduced into the

United States (Anderson et al., 2017), including Chlorocebus. Florida is home to three introduced primates: Saimiri sciureus (squirrel monkey), C. sabaeus (green monkey), and

Macaca mulatta (rhesus macaque). All three species were introduced through various zoos, research facilities, private collections, and entertainment businesses (Anderson et al., 2017; Layne, 1997; Westley, 1950; Wolfe & Peters, 1987). Some of the impacts of the established primate populations are harmless, whereas others are more serious, such as potential threats to human health, destruction of environmental resources, and economic loss (Anderson et al., 2017; Wisely et al., 2018).

Early media reports state that the monkeys of Dania Beach, Florida have been part of the local community since the 1950s (Banker, 1991). However, the origins of the

Dania Beach monkey population are unknown due to lack of official documents. Local folklore suggests that the monkeys either escaped or were released from a failed roadside zoo or tourist attraction in the mid-1950s and early 1970s (Hyler, 1995). The only documented zoo or tourist attraction historically in Dania Beach to house primates was the Dania Chimpanzee Farm, formerly the Anthropoid Ape Research Foundation

(Schindler, 1946).

There has been only one systematic field study completed on the population

4 (Hyler, 1995). One aim of Hyler’s study, an undergraduate thesis at Florida Atlantic

University, was on the possible geographic origins of the population based on morphology (southern and western Uganda). Hyler referred to the monkeys as

Cercopithecus aethiops, however suggested that monkeys maybe hybrid between

Cercopithecus pygerythrus and Cercopithecus tantalus. He reached this conclusion by comparing his study photographs to those of Dorst (1970) and Kingdon (1971). Currently the taxonomic classification within this genus is inconsistent, well represented by the

FWC website that identifies the population as both Chlorocebus pygerythrus and

Chlorocebus aethiops.

The taxonomy of this genus in the 1970s was less understood, lumping vervet monkeys together with other African primates (guenons) in the genus Cercopithecus

(Lernould, 1988). Recently all vervet monkeys were moved from the genus

Cercopithecus to a new genus, Chlorocebus (Groves, 2001). There are six species

(aethiops, sabaeus, tantalus, pygerythrus, cynosuros, and djamdjamensis) represented within the genus Chlorocebus, but often commonly referred to a Chlorocebus aethiops in the literature (Groves, 2005; Grubb et al., 2003). Groves used current findings on genetics, morphology, and ecology for the classification of the six species into the genus

Chlorocebus (Groves, 2001, 2005). The IUCN (2019) currently uses this taxonomic classification as well to describe vervet monkeys.

Vervets are the most widespread of the African monkeys and are habitat generalists, limited only by the availability of water and sleeping trees (Pasternak et al.,

2013; Wolfheim, 1983). Species within Chlorocebus have bluish skin on their abdomens with black faces, hands and feet (Groves, 2001). There is variation of hair color within

5 the genus ranging from greenish-brown hair to grayish olive hair (Gaetano, 2012). Males have a blue scrotum and red penis and perianus surrounded by white hair (Gaetano,

2012). These are exposed during dominance displays and are referred to as a “red, white, and blue display” (Struhsaker, 1967a). The shade of the blue scrotum varies within species from a bright turquoise blue to a pale blue (Cramer et al., 2013; Gaetano, 2012).

They are ubiquitous in labs due to their abundance in the wild, typically are disease-free, and easy to handle (Jasinska et al., 2013). They have also been the focus of ethnoprimatology studies due to their ability to live alongside humans (Dore, 2013; Guy,

Stone, & Curnoe, 2012; Patterson et al., 2017; Patterson, Kalle, & Downs, 2018).

This study aimed to confirm the study species and origins of the Dania Beach monkeys, as it is unknown due to the lack of official documents. Mainstream media sources suggested that the monkeys escaped from the Anthropoid Ape Research

Foundation, also known as the Dania Chimpanzee Farm (Banker, 1991). Various historical archives state that the facility imported primates from Africa to be sold to research facilities (Montayne, 1946). There is also the possibility of a source population in the Caribbean, although this is not mentioned in local media records.

There is a lack of consensus on the taxonomic classification of the Dania Beach monkey population. Currently the FWC labels the population as two different species

(aethiops and pygerythrus). Accurate identification of the population would allow the

FWC to educate the public and help guide management protocols. Taxonomy is best done with multiple lines of evidence through pelage (i.e., Hyler’s morphology assessment), genetics, and historical records. This study followed such an integrative taxonomic approach (e.g., Padial, Miralles, De la Riva, & Vences, 2010) to infer the origins and

6 taxonomic identity of the Dania Beach monkeys. Based on initial phenotypic observation coupled with past media records, we tested the hypothesis of West African C. sabaeus origins with the addition of genetic analysis. If the Dania Beach genetic data do not show support for West African C. sabaeus, it suggests that the monkeys could be of Caribbean origins or a mix of both African and Caribbean populations. If there is support for

Caribbean genetic origins, we will search for documentation to corroborate findings.

Methods

Phenotype analysis. The monkeys of Dania Beach were photographed to create a database of all individuals (n = 36). Photographs were taken using a hand held Canon

Rebel EOS 13 with a 55-255 mm lens. We took photos of individuals during daylight hours at various times throughout the day to account for variability in natural lighting at a distance of 1-3 meters. We recorded the following traits to help identify species of monkey: 1) color of pelage, 2) presence or absence of brow band, 3) color of tail tip, and

4) scrotum color of males. These attributes were then compared to all species within the genus Chlorocebus to determine study species (see Table 1).

7 Table 1

Summary of Pelage Color Variation Across Species of Chlorocebus

Species Pelage Color Description

Bale monkey, The dorsal body is covered by a longer, brownish hair with shorter whiskers Chlorocebus and shorter black tipped tail. A long white hair beard surrounds a black face djamdjamensis with a faint, white brown band separating face from dorsal hair. Males have a pale blue scrotum.

Green monkey, Black face framed by yellow-golden whiskers with a bib of long reddish- Chlorocebus sabaeus yellow hair. The dorsal is greenish-brown and yellow, with a golden yellow tail tip. Lack whitish brow band on brow. Males have a pale blue scrotum

Grivet monkey, Dorsal has pale grayish-olive hair with elongated white whiskers and white Chlorocebus aethiops moustache framing black face. A white frontal brow band separates the short hair of the face from the longer hairs of head and body, and a tan tip tail. Males have a sky-blue scrotum.

Malbrouck monkey, White hairs form a bonnet around a slightly depigmented face with bald rings Chlorocebus around the eyes. Short grayish-olive hair covers the dorsal body and head, with cynosuros ears exposed. They have black hands and feet. Males have an azure blue scrotum.

Tantalus monkey, Black face framed by long whitish hairs to cover ears. White brow band is Chlorocebus tantalus separated by whiskers of black temporal bar Dorsal body is live with a white caudal tuft and white tip tail. Males have a sky-blue scrotum.

Vervet monkey, Dorsal body has grayish-yellow hair extending to tail with a black tip tail. Chlorocebus Black face is surrounded by a long white hair extending to the throat and pygerythrus stomach. Males have a turquoise blue scrotum. Note. Adapted from Gaetano (2012).

Historical data collection. I used semi-structured public interviews, literature reviews, and historic and current popular media (including social media) content to collect historical information on the green monkey population. I used Web of Science to search the peer reviewed literature using relevant terms. My search included state agency reports, book chapters, and university theses. We used Google to search for media articles and videos using terms such as “Dania Beach monkey,” “Dania Beach vervet,”

“introduced monkeys Dania Beach,” “introduced monkeys Florida,” and “introduced vervets Florida.” Google search results included local and national news agencies,

8 historical community archives, YouTube videos, Facebook posts, and documentaries. I conducted semi-structured interviews with local community members who had knowledge of the vervet population (Bernard, 2006). Interview questions focused on the origins of the monkeys, how the monkeys were introduced to area, how many monkeys historically were introduced, and why the monkeys were imported to Florida.

Genetic analysis.

Sample collection. With the approval of Florida Atlantic University’s Institutional

Animal Care and Use Committee, I collected five fecal samples and one tissue sample from the introduced C. sabaeus population in Dania Beach, Florida (2015-2017). The fecal samples were kept in RNAlater preservative and stored in the -20 °C refrigerator for long term preservation. During our study a male juvenile monkey was struck by a car, we extracted DNA from his carcass by snipping his ear and stored the remainder of his remains in the -20°C freezer.

DNA extraction, amplification, and sequencing. Total genomic DNA was extracted from the five fecal samples by using the QIAmp DNA Stool Extraction Kit from Qiagen. To extract total genomic DNA from the tissue sample, we used the DNeasy

Blood & Tissue Kit from Qiagen. Standard protocol was followed provided by Qiagen for the extractions, except for minor modifications done for the extraction of fecal and tissue samples. The fecal and tissue sample extracts were stored in the -20°C freezer in aliquots for up to 12 months before further handling.

Two genetic markers were used from the mitochondrial genome to estimate the geographic origins of the population (Avise, 2009). The whole cyt b gene (1,140 bp) was amplified by using five overlapping fragments (Haus et al., 2013) yield the best results

9 from the degraded DNA in the fecal samples and a 602 bp long fragment (Mekonnen et al., 2018) of the HV1 region.1 U GoTaq G2 Green Master Mix, 0.33-µM was used for each primer (forward and reverse), 2-µl of genomic DNA, and 8.86-µl ddH20 (HV1) and

6.5-µl ddH20 (cyt b) in a 25-µl final volume PCR mix. The PCR conditions followed the procedure recommended by Haus et al. (2013) and Mekonnen et al. (2018), 94°C for 2 minutes, followed by 40 cycles of 94°C for 1 minute, 62°C (cyt b) and 54°C (HV1) for 1 minute, 72°C for 5 minutes.

For the Y-chromosome analyses, two Y-chr genes were amplified and sequenced: a 783 bp long overlapping fragment of the sex-determining region (SRY) and a 695 bp overlapping fragment of the last intron of the zinc finger (ZFY) (Haus et al., 2013). 1 U

GoTaq G2 Green Master Mix, 0.33-µM was used for each primer (forward and reverse),

2-µl of genomic DNA, and 6.5-µl ddH20 in a 25-µl final volume PCR mix. The PCR conditions followed the procedure recommended by Haus et al. (2013), 94 °C for 10 min, followed by 35 cycles of 92°C for 30 sec, 50°C for 30 sec, 72°C for 30 sec, and 72°C for

15 min. All PCR products were run on 2% agarose gels, then purified with the QIAquick

Qiagen PCR Purification Kit and sent off for sequencing along with the amplification primers to Molecular Cloning Laboratories in San Francisco, California.

Taxon sampling. For the final alignment of the mtDNA genes, 11 African green monkeys were added with unique haplotypes and Erythrocebus patas as the outgroup from GenBank, and one representative from the Dania Beach population, SU17DM17.1.

For the final Y-Chr. alignment, African green monkeys were added with unique haplotypes and Papio hamadryas as the outgroup from GenBank, and the same representative from Dania Beach, SU17DM17.1. Different outgroups were used as a

10 result of incomplete Y-chr. gene sequences available on GenBank for Erythrocebus patas.

Statistical analysis. The chromatograms were inspected for accurate base calls by eye and assembled them by using Geneious R11 (Kearse et al., 2012). From the six samples, one representative, SU17DM17.1 was brought into the cyt b, HV1, ZFY, and

SRY alignment. Each sequence was aligned with MUSCLE 3.8.3 algorithm in MEGA

7.0.14. (Kumar, Stecher, & Tamura, 2016). Two separate alignments were constructed through SequenceMatrix 1.8 (Meier, Shiyang, Vaidya, & Ng, 2006), one concatenated alignment of the two mtDNA markers HV1 and cyt b, and a second alignment of the two

Y-chr markers ZFY and SRY. The appropriate best-fit nucleotide substitution model was chosen for each gene partition in the two alignments, (HKY + G for cyt b and HV1, JC for SRY, and HKY for ZFY) through PartitionFinder2 (Lanfear, Frandsen, Wright,

Senfeld, & Calcott, 2016) on the CIPRES cluster (Miller, Pfeiffer, & Schwartz, 2010) using the Bayesian Information Criterion (BIC). Bayesian and maximum-likelihood (ML) methods were used for phylogenetic tree reconstruction using the programs MrBayes

3.2.6 (Huelsenbeck & Ronquist, 2005) and Garli 2.01 (Zwickl, 2006), respectively. For the Bayesian inference analysis, we applied 5,000,000 generations sampled every 1,000 generations. The first 25% of sampled trees and parameters were discarded as burn in from the output. For the ML analysis, each gene was partitioned for 500 bootstrap replications and four independent runs to calculate relative support values of internal nodes, all other parameters were left at their default settings. A 50% majority-rule consensus tree was computed with PAUP* 5.0 (Swofford, 2011) to obtain bootstrap percentages. A consensus tree was uploaded into the program FigTree v1.4.3 (Rambaut,

11 2016) to view both analyses. The trees were exported into Inkscape v.0.92

(https://inkscape.org) to make them publication ready. MEGA 7.0 (Kumar et al., 2016) was used to calculate nucleotide and haplotype diversity among the Chlorocebus dataset.

Results

Phenotype observations. The monkeys in Dania Beach have a golden tipped tail and greenish-brown hair, lack a pronounced brow band around the face, and males have a pale blue scrotum (see Figure 2). These phenotypic traits are characteristic of C. sabaeus

(Gaetano, 2012; Groves, 2001, 2005). This species is commonly referred to as a green monkey because of the pelage color (Groves, 2001, 2005). Green monkeys are endemic to West Africa, with a range from Senegal and Guinea-Bissau west into Ghana (Gonedelé

Bi et al., in press) (see Figure 1).

12

Figure 1. Distribution of African green monkeys (Chlorocebus spp.). Map is modified with permission from Haus et al. (2013).

13

Figure 2. Dania Beach monkeys photographed during this study. Top left photo: Adult male (Dania Beach) black face without brow band, surrounded by yellowish whiskers. Bottom left photo: Adult male (Dania Beach) pale blue scrotum. Right side photo: Adult male (Dania Beach) with greenish-olive pelage and golden yellow tipped tail.

History. The historical research from this study confirms the source of the Dania

Beach monkey population traces back to an escape from the Anthropoid Ape Research

Foundation. Leila Roosevelt Denis (first cousin of Theodore Roosevelt and second cousin to Mrs. Franklin D. Roosevelt) and her Belgian borne husband, Armand Denis, Sr. purchased the Thunderbird Indian Trading Post in 1939 and renamed it the Anthropoid

Ape Research Foundation (Cunningham, 2011; Schorer, 1948). This property was located

14 directly north of the Dania Cut-off Canal on Federal Highway in Dania Beach. The facility acted as a zoo and, also provided primates imported from Africa as research subjects in the development of the polio vaccine and other medical research. The species and quantity of primates imported is unknown. However, an article in the Philadelphia

Inquirer reported 300 monkeys, 50 chimpanzees, and other wildlife living on the property in 1948 (Schorer, 1948). In 1949 John and Dorothy Ash bought the property and renamed it the Dania Chimpanzee Farm. It was reported that they continued to import primates for medical and entertainment purposes. The primates were sold to Dr. Salk and Dr. Sabin for polio research, John Hopkins University for tuberculosis research, National Institutes of Health for infectious disease research, and the United States Air Force for early space travel research (Cunningham, 2011).

According to a former Dania Chimpanzee Farm employee, Peter Karsner, various types of primates were housed at the Dania Chimpanzee Farm, including chimpanzees, mandrills, red tailed monkeys, and vervets (P. Karsner, personal communication,

September 28, 2014). He also recalled that various types of monkeys did escape into the surrounding mangroves, however, the vervets were the only ones to survive. Bill Westley was employed by the foundation in 1944 to travel to Africa to collect primates. He reported the collection of animals in the book, Chimp on My Shoulder (Westley, 1950).

His journey started in Sierra Leone and ended in the Congo. While traveling through

Africa, he described collecting green monkeys, among other Old World Monkeys, and chimpanzees that were shipped back to Dania Beach, Florida (Westley, 1950). While in

Freetown, Sierra Leone, Westley stated that “Most of the monkeys were tough little

African Greens, so called because their hair is definitely gray-green” (p. 158). He further

15 described that he hired locals to capture the monkeys for shipment back to the

Anthropoid Ape Research Foundation (Westley, 1950).

In 1994, Dale Minnich produced a documentary, The Dania Monkey Story. He explored the Dania Beach monkey origins, interviewed former zoo employees and community members about the local monkey population. The documentary provided corroborative evidence of the historical archives about the monkey population’s history and escape. A former animal handler at the Dania Chimpanzee Farm, Kenneth McDougal

(now deceased), stated in the documentary that the monkeys were housed in an aviary type enclosure secured only with a screen door hook. In 1947 all of the monkeys

(estimated 50) escaped into the surrounding mangrove forests either due to a zookeeper that failed to lock the door or a monkey who opened the lock. All but approximately 12-

15 monkeys were caught. McDougal reported that the monkeys would come into the zoo at night to steal food from other animals’ enclosures. Eventually the monkeys moved deeper into the mangroves and stopped returning to the zoo. Former Dania Beach mayor and Dania Beach historian, Charles “Mac” McElyea, was interviewed as well. He stated the Dania Chimpanzee Farm was used primarily for primate medical research needs however that facility was a tourist attraction (see Figure 3). Additionally, he said the monkeys were housed at the facility (Minnich, 1994).

16

Figure 3. Dania, Florida Chimp Farm brochure, circa 1950s.

Genetics. Phylogenetic analyses confirmed that the Dania Beach monkey group with C. sabaeus (green monkey) have West African origins. There was consensus among the trees generated from the two alignments (see Figures 4 & 5). The nuclear and mitochondrial datasets were kept separately because of their different evolutionary

17 histories (Roos et al., 2011). No variation among the sequences from the (n = 6) individuals sampled, as all individuals within the population shared the same haplotype for cyt b, HV1, ZFY, and SRY.

Figure 4. Bayesian phylogram depicting Bayesian posterior probability values and ML bootstrap support values based on the concatenation of the sex determining region (SRY) and the last intron of the zinc finger (ZFY) gene on the Y-chromosome. Posterior probability values of 1.00 and bootstrap support values of 100% are presented by asterisks; values below are provided at respective nodes. Tip labels consist of species name, country of origin in abbreviation, followed by the last three digits of each sample’s accession number. Our individual specimen is demarked in red, followed by country and lab ID number.

18

Figure 5. Bayesian phylogram depicting Bayesian posterior probability values and ML bootstrap support values based on the concatenation of a 602 bp fragment of the hypervariable region 1 (HV1) and the complete cyt b gene from the mitochondrial genome. Posterior probability values of 1.00 and bootstrap support values of 100% are presented by asterisks; values below are provided at respective nodes. Tip labels consist of species name, country of origin in abbreviation, followed by the last three digits of each sample’s accession number. Our individual specimen is demarked in blue, followed by country and lab ID number.

Discussion

This study confirms the historical and geographic origins of the Dania Beach green monkey population. Archival data corroborated our phenotypic predictions and genetic findings to confirm the monkeys of Dania Beach to be C. sabaeus. The monkeys

19 were imported to Florida from Africa due to the demand for primates in medical research in the 1940s. Primates were used for polio research, tuberculosis studies, and infectious diseases during this time period (Cunningham, 2011). Primates from the facility were shipped to John Hopkins University, National Institutes of Health, and the Air Force (for studies of the sound barrier and space travel) (Cunningham, 2011).

The genetic findings were limited to species identification through the use of four markers: the mtDNA cyt-B gene and mtDNA HV1 region, and two Y-chromosome loci.

The mtDNA cyt-B gene is a highly conserved marker that is used for species identification (Avise, 2004). The Y-chromosome markers (SRY and ZFY) provided paternal evolutionary history. Specifically relevant to this study, recent research provides excellent comparative data for these two markers which increased our ability to understand population origins (Haus et al., 2013; Svardal et al., 2017). All markers provided strong support for West African origin and taxonomic identification as C. sabaeus. The concatenated mtDNA cyt-b gene and HV1 region from the Dania Beach sample grouped closest with the sabaeus sample from Sierra Leone. Although the concatenated Y-chromosome markers did not yield a result with a high resolution at the population level, the analysis provided 100% statistical support for grouping within C. sabaeus.

The genetic variation of the initial founding population and current population in

Dania Beach is unknown. However, we speculated that green monkeys were caught in various parts of West Africa due to the travel Westley (1950) described in his book.

Westley reported that he obtained 14 chimps and 170 monkeys that were intended for shipment to the AARF. However, he did not clarify as to what various monkey species

20 were included in his cargo. Based on this information, we assume that the monkeys that escaped into the mangroves were a mixed group of individuals caught from different green monkey populations from West Africa. Additional genetic research with more loci is needed to estimate the variation within the population and level of inbreeding. Further analysis can be done through the comparative studies of published genomic data of

Chlorocebus from different African and Caribbean populations (Svardal et al., 2017).

This study contributes to the FWC’s knowledge about the monkey population in

Dania Beach. Currently the species is listed as aethiops and pygerythrus. The correct identification of an introduced species is crucial to wildlife agencies to better understand any potential impact and how best to develop management policies (Simberloff, 2003;

Simberloff et al., 2005; Wright, Eberhard, Hobson, Avery, & Russello, 2010). Further, correct public information is important as management decisions can be influenced by public opinion (Chauhan & Pirta, 2010; Decker et al., 2013). Our study contributes both to the wildlife management and scientific communities through the species identification of the monkeys in Dania Beach, Florida.

21 CHAPTER 2. DEMOGRAPHICS AND POPULATION VIABILITY ANALYSIS

Introduction

Humans have been introducing primates into new habitats for at least 500 years, including zoogeographic regions where primates had not existed previously (Anderson et al., 2017; Riley & Wade, 2016). Evidence suggests that primates can persist outside of their native regions in environments with diverse climates, habitats, food sources and availability, predators, and native fauna (Riley & Wade, 2016). The survival of introduced primates depends on the ability of the species to use the habitat and disperse to increase its population size in the new location (Riley & Wade, 2016). Climatic conditions have profound effects on food availability and impact the ability of introduced primates to survive by incorporating new foods into their diet (Coleman & Hill, 2015;

Riley & Wade, 2016). Most of the successfully introduced primate taxa, including members of the genera Macaca, Papio, and Chlorocebus, are known for their ecological flexibility and are considered generalists (Barrett, 2005; Riley & Wade, 2016). Since the

1930s, at least 10 species of primates have been introduced into the United States

(Anderson et al., 2017), including Chlorocebus.

The genus Chlorocebus includes six species and is widespread throughout sub-

Saharan Africa (Kingdon, 2015). The adaptable nature of Chlorocebus monkeys, along with their ability to learn quickly and change their behavior accordingly, allows them to be successful when living close to humans (Else, 1991). Consequently, Chlorocebus species have become agricultural pests in Africa and in the Caribbean, where they

22 were introduced during the slave trade in the 1600s (Dore, 2013; Gaetano et al., 2014;

Patterson et al., 2017, 2018).

Populations of C. sabaeus (green monkey) have been established on three islands in the Caribbean: Barbados, St. Kitts, and Nevis (Anderson et al., 2017; Horrocks, 1986;

Hyler, 1995). In response to the green monkeys’ nuisance behaviors, Barbados and St.

Kitts developed culling programs to reduce the monkey populations Chapman & Fedigan,

1984; Horrocks & Baulu, 1988). Despite land development and culling, the green monkey population grew 300% over the course of one decade on St. Kitts (Chapman &

Fedigan, 1984). In 1980, Barbados started a 7-year trapping program intended to manage the green monkey population (Horrocks & Baulu, 1988). The number of green monkeys trapped annually in Barbados increased from less than 200 individuals in 1980 to 1,000 individuals in 1986, but the trapping had no evident impact on the overall population size

(Horrocks & Baulu, 1988). Despite the removal of over 10,000 green monkeys via hunting and humane trapping from 1980 to 1994, the green monkey population size in

Barbados in 1994 remained stable over that period (Boulton, Horrocks, & Baulu, 1996).

These studies show that green monkeys flourish in marginal and human-disturbed habitats despite removal efforts (Brennan, 1985; Hill, 2000; Kavanagh, 1980).

Since the 1930s, at least 10 species of primates have been introduced into the

United States (Anderson et al., 2017), including Chlorocebus. Florida is home to three introduced primates: Saimiri sciureus (squirrel monkey) in Broward County, C. sabaeus

(green monkey) in Broward County, and Macaca mulatta (rhesus macaque) in Marion

County. All three species were introduced through various zoos, research facilities, private collections, and entertainment businesses (Anderson et al., 2017; Layne, 1997;

23 Westley, 1950; Wolfe & Peters, 1987). Some of the impacts of the established primate populations are harmless, whereas others are more serious, such as potential threats to human health, destruction of environmental resources, and economic loss (Anderson et al., 2017; Wisely et al., 2018).

This study focused on the introduced C. sabaeus population in Dania Beach,

Florida. In this paper, we use the common name green monkey, as recommended by the

African Primate Specialist Group of the IUCN Red List (Kingdon & Gippoliti, 2008); however, the common name, vervet, is more frequently used by the local communities and media (Fleshler, 2015; Stevens & Powell, 2015). The population was founded in

1947 from the Anthropoid Ape Research Foundation, which imported green monkeys from Africa to Dania Beach during the 1940s for medical purposes (P. Karsner, personal communication, September 28, 2014; Westley, 1950). The population is well known by the local human community, but there is limited scientific information available. Only one systematic survey conducted in 1991-1992 has provided census data for the Dania

Beach green monkey population (Hyler, 1995). This survey occurred in West Lake Park

(WLP), Dania Beach at the request of Broward County Parks and Recreation and documented a total population size of 36 monkeys. It is unknown whether the population is growing or declining and whether it is spreading.

The high population growth and complex problems of the introduced populations of green monkeys in the Caribbean (Dore, 2013) raise important questions about the current status and future trajectory of the Dania Beach green monkey population. Unlike the reported single Dania Beach monkey introduction event, it is assumed that there were multiple introductions (escaped or released pets) to the Caribbean islands due to English

24 and French settlers, and the slave trade from West Africa during the 1600s (Dore, 2017;

McGuire, 1974). The islands were composed of relatively undisturbed habitat with an abundant food supply that offered an ideal environment for population growth for a highly adaptable primate species (McGuire, 1974).

Today the monkey population continues to thrive in the Caribbean despite anthropogenic influences of agricultural development, urban expansion, and culling.

Historically, Dania Beach has been primarily an agricultural landscape (Kemper, 1979).

Dania Beach was more developed compared to the Caribbean Islands when the monkeys were presumably introduced in Florida; however, there were agricultural areas available and natural spaces for the animals to exploit. This available habitat provided a conducive habitat to encourage the population growth documented in the Caribbean.

The purpose of this study was to evaluate population growth and analyze population viability. We conducted a longitudinal study of the Dania Beach population to measure demographic parameters and determine population growth and viability. We used a population viability analysis (PVA) tool to assess the population’s trajectory and viability (Smith, King, Campbell, Cheyne, & Nijman, 2018). PVA uses mathematical simulations to estimate wildlife population viability in the face of different deterministic forces and stochastic events over time (Smith et al., 2018). We predicted population growth of the green monkeys in Dania Beach due to their ecological and behavioral plasticity. If the population is adapted to the mangrove habitat, then population trends should demonstrate growth or stability, which will be reflected in demographic data.

25 Methods

Study site. We collected demographic data from January 2014 through April

2018 in Dania Beach, Florida, on local business parking lots, private land, the Lake

Mabel section of WLP, and adjacent federally secured land on Port Everglades. West

Lake Park is a 1500-acre nature preserve located in southeastern Broward County within the cities of Hollywood and Dania Beach (see Figure 6). West Lake is the largest remaining mangrove ecosystem in the 85-mile, highly developed urban coastal zone from

Miami Beach to West Palm Beach (Broward County Government, 2019). Major roads and planned communities border the park on the east, west, and south, and the Dania Cut- off Canal is located to the north. In addition to the major roads and urban community, the

Fort Lauderdale-Hollywood International Airport is west of Lake Mabel. Recent expansion of the airport runway has intruded into the mangrove habitat, increasing the number of reported sightings of monkeys on the airport tarmac.

26

Figure 6. West Lake Park, Dania Beach, Florida (Broward County Government, 2018).

The WLP mangrove ecosystem is home to various reptiles (e.g., water snakes, lizards, and turtles), birds (e.g., water birds, hawks, and vultures), amphibians, and

27 mammals (e.g., coyotes and raccoons). The salinity of the park’s water is 30 parts per thousand (16). Predominant plant species include red mangroves (Rhizophora mangle), white mangroves (Laguncularia racemosa), and black mangroves (Avicennia germinans).

Drainage canals and mosquito-control ditches are distributed throughout the park area

(Hyler, 1995). The South Florida region has a tropical savanna environment with a defined rainy season from May through October and an average annual rainfall of 169 cm

(33). The average high temperature is 28.3°C, and the average low is 19.4°C, with an annual average temperature of 23.9°C (U.S. Climate Data, 2019).

Demographic data collection. We conducted 529 site visits from January 2014-

April 2018 at four different locations where monkeys had been reported by the businesses and wildlife authorities. We observed the monkeys for a total of 540 hours, with an average of 135 hours at each site during the study period. Because the monkeys are fed by humans, provisioned social groups were tolerant to observation at provisioning sites.

This allowed us to identify members of the population. We used physical attributes to identify individuals, including facial depigmentation patterns, scars, and missing limbs.

We created a photo database to maintain records of the individual monkeys. We documented illnesses, injuries, births, deaths, disappearances, immigrations, emigrations, and group counts during site visits. Each social group’s location was determined by GPS and noted every 15 minutes, along with the group’s size and composition. The physical challenges of the mangrove habitat limited our observations to parking lots and walkable sections of the swamps.

We classified the monkeys by sex and age. The age classes were: adults (females

> 48 months and males > 60 months), female juveniles (12-48 months) and male

28 juveniles (12-60 months), and infants (< 12 months) (Cheney, Seyfarth, Andelman, &

Lee, 1988). Previous studies of C. sabaeus showed that males and females typically achieve adult status at 5 and 4 years of age, respectively, and that females first give birth at around 5 years of age (Cheney et al., 1988; Fairbanks & McGuire, 1984; Horrocks,

1986). We identified adult males by the presence of a full pale blue scrotum and adult females by the presence of elongated nipples (Horrocks, 1986; Isbell, Young, Jaffe,

Carlson, & Chancellor, 2009). We identified infants by their nursing behavior and facial coloring (Krige & Lucas, 1975; Lee, 1984; Struhsaker, 1971). We recorded birth events observed during the study period. We estimated the infant birth dates to within 72 hours based on the last time the female was recorded as being pregnant.

We classified mortality events based on previous vervet mortality studies (Cheney et al., 1988; Isbell, 1990). A death due to illness meant that an animal disappeared within

24 hours of having been observed as weak, severely injured, or diseased (Cheney et al.,

1988). A confirmed death meant that we observed a deceased animal, or an animal being killed (Cheney et al., 1988). A disappearance meant that an animal was absent for more than 24 hours for an unknown reason (Isbell, 1990). If an adult male was absent for more than 72 hours, we considered it a dispersal event, not a mortality event, unless we found remains of the animal or the animal’s previous physical appearance indicated a decline in health. Because adult females and juveniles of either sex rarely move among social groups (Cheney, Lee, & Seyfarth, 1981), we classified events where those individuals went missing as disappearances if no cause was determined (see Appendix A).

Statistical analysis. We conducted descriptive statistics [mean and standard deviation (SD)] and Pearson’s linear correlation test (two-tailed, with statistical

29 significance set at p = 0.05) using VassarStats: Website for Statistical Computation

(Lowry, 2019). We analyzed the viability of the Dania Beach vervet population using

Vortex 10 population viability analysis software, which is designed for species with low fecundity and long lifespans (Lacy & Pollack, 2014). Vortex models the effects of deterministic forces as well as environmental, demographic, and stochastic genetic events

(Smith et al., 2018). We based the model parameters on our demographic data, knowledge of the population and environment, as well as published data on Chlorocebus

(see Table 2). We created five different model scenarios to examine the effects of different variables on the population (see Table 3). We ran each scenario 1000 times.

Scenarios S1–S4 modeled the population over a 26-year period starting with the parameters measured in the 1992 census. We compared the population sizes at the ends of these scenarios (S1-S4) to the current population size as measured by our survey in

2018. In scenarios S2 and S4, we included harvesting events (to model the effects of trapping). In S3 we added another social group to see if those variables had a significant impact on the model. There have been anecdotal reports of trapping events for the pet trade; in 1995, for example, there was a report of an exotic pet dealer using blow darts to catch Dania Beach green monkeys (Harakas, 1995). Because the 1992 census was limited to WLP, it is possible that a social group was missed because it was outside the confines of the park. For example, one business owner north of the WLP boundary reported monkeys on his property during the 1990s. Therefore, scenarios 3 and 4 included an additional social group to account for this information. Scenario S5 differed from scenarios 1-4 in that it modeled hypothetical population growth within the next 100 years based on the current demographic data. Lastly, we also ran S1 for 100 years based on

30 Hyler’s data to model predicted population growth. To test for change in output results, we modified the percent of adult females breeding by increments of 10% in S5.

31 Table 2

Vortex Model Parameters

Parameter Input Value Rationale Inbreeding depression Software default There is limited information on inbreeding depression settings: 6.29 in wild vervet populations. Lethal equivalents: 50% due to recessive lethal alleles Breeding system polygynous Vervets live in multi-male/multi-female units (Struhsaker, 1967b). Age at first 4/5 Average age of first reproduction in wild populations reproduction in years, (Cheney et al., 1988; Horrocks, 1986; Isbell et al., females/males 2009; Struhsaker, 1971. Percent of adult 56% (SD +/- 14) Represents females in the current population that females breeding reproduced annually 2014–2018. (standard deviation) Maximum number of 1 Vervets give birth to one infant per year. broods per year Maximum number of 1 Vervets typically give birth to one infant; twins are progeny per brood rare. Maximum age at 20/25 Female fecundity slows at the age of 16 (Atkins at al., reproduction in years, 2014; Isbell et al., 2009). Males can reproduce until female/males death. Known male maximum lifespan up to 25 years. Sex ratio of births 50/50 Reported average ratio is wild population studies (Hoorocks, 1986). Mortality rates for all 0-1 years: 31% (15) Mortality rates are based on the life table analysis of age classes (standard 1-2 years: 36% (15) the infant cohort born Jan. 2014–Jan. 2018 and the deviation in estimated ages of individuals present within the 2-3 years: 0% (0) parentheses) population at the start of the project. The Vortex scant 3-4 years: 15% (49) method was used to calculate standard deviations for 4-5 years: 14% (49) age classes 3+ years because of minimal demographic 5+ years: (Female): data. 9% (4) 5+ years: (Male): 19% (4) Initial population size 36 Based on demographic data from 1992 (Hyler, 1995). Carrying capacity 200 Based on other vervet demographic studies (Boulton et al., 1996; Hall & Gartlan, 1965; Horrocks, 1986; Horrocks & Baulu, 1988). Mate monopolization 22% Represents all adult males in the 1992 census. Harvest 1 infant male, 1 Based on anecdotal trapping reports. infant female

32 Table 3

Description of the Five Different Modeling Scenarios

Scenario Description

S1 1992 census data with no harvest.

S2 1992 census data with annual harvest of infants (1 female, 1 male).

S3 1992 census data with an additional social group of 12 individuals, no harvest.

S4 1992 census data with an additional social group of 12 individuals with annual harvest (1 female, 1 male).

S5 January 2018 census data with 100-year time frame.

We defined the population as the combination of all social groups of green monkeys within and near the park boundaries of WLP. We considered the population extinct when only one sex remained at any time during the scenario. We included inbreeding depression using the default settings in Vortex, as there is limited specific information on inbreeding depression in Chlorocebus. We did not include catastrophes in the model parameters because there is no available information about the impact of disease or natural disasters on wild Chlorocebus populations. We set the carrying capacity at 200 individuals for the 1500 acres of unoccupied natural space in WLP.

Previous studies have shown that a high number of vervets can occupy a small area; for example on Lolui Island, Lake Victoria, the population density was 225 individuals per square mile (Gartlan, 1969), and on the island of St. Kitts it is estimated that there are

30,000 vervets on 69 square miles (Turner, Cramer, Nisbett, & Patrick Gray, 2016).

We used our survey data to calculate population-specific parameters of sex ratio, mortality rate, number of breeding females, and male mate monopolization for the models. We calculated the proportional mean number of females breeding by dividing the

33 total number of infants born by the total number of adult females per year. We calculated the proportion of adult males by dividing the total number of adult males by the total number of individuals within the population. Vervets are polygynous breeders, so any adult male has the potential to mate. We calculated the interbirth interval (IBI) by determining the number of days between the calendar dates of sequential births and converting back into months using 30.4 days to represent one month (Fairbanks &

McGuire, 1984).

After we ran each scenario 1000 times, we recorded the probability of extinction

(PE), deterministic growth rate (det-r), mean stochastic growth rate (stoc-r), mean time to extinction (TE), mean number of individuals surviving each simulation (extant N), and the standard deviation for each variable. The det-r is the projected growth rate excluding stochastic events (Stark, Nijman, Lhota, Robins, & Goossens, 2012). A population is considered stable if the stoc-r is close to the det-r; it is considered unstable if the stoc-r is less than the det-r (Smith et al., 2018).

Results

Group size and social structure. Our census data reflected 6-month intervals that began in January 2014 (see Table 4). Initially, only one social group (P2) was found in January 2014. After exploring the mangroves and surrounding businesses, we documented the additional social groups (P1, M3, and M4) in March 2014. Our last census in January 2018 showed a 13.8% increase in the overall population size (N = 41) compared with the 1992 census data (N = 36).

34 Table 4

Total Number of Individuals Within Each Social Group 2014–2018

Group Jan. June Jan. June Jan. June Jan. June Jan. 2014 2014 2015 2015 2016 2016 2017 2017 2018

P1 12 13 12 11 12 17 16 19

P2 11 12 14 15 19 19 16 17 17

M3 7 8 7 8 8 5 5 3

M4 2 1 1 1 1 2 2 2

Total 11 33 36 35 39 40 40 40 41

We observed the Dania Beach green monkeys in stable social groups (groups of two or more interacting individuals) that ranged in size from 2 to 19 individuals. From

January 2014 to April 2018, we documented a total of 64 individuals distributed among four social groups: P1, P2, M3, and M4. The mean group size over the entire study period was 10.25 individuals, which represented a 43% reduction compared with the mean group size of 18 individuals reported in 1992 (Hyler, 1995) (see Table 5). The mean group size of the Dania Beach C. sabaeus population was smaller than that of other C. sabaeus populations in Senegal (n = 11.8) and Barbados (n = 15.3) (Dunbar, 1974;

Horrocks, 1986). The social groups were distributed throughout the northernmost section of WLP, Port Everglades federal land, adjacent businesses, and private land. Two of the social groups (M3 and M4) were in the same locations where two social groups comprising a total of 36 individuals were reported in 1992 (Hyler, 1995).

35 Table 5

Vervet Social Group Sizes Across Different Locations and Studies

Species Group Size Habitat Site Author

C. aethiops 12.7 Mixed Lolui Island, Lake Hall & Gartlan (1965) Victoria

C. aethiops 24.1 Savanna Amboseli National Park, Struhsaker (1967b) Kenya

C. sabaeus 11.8 Mixed Parc National du Niokolo- Dunbar (1974) Koba

C. aethiops 18.3 Urban/Natural Burman Bush, South Henzi & Lucas (1980) Africa

C. aethiops 15.3 Savanna Amboseli National Park, Cheney & Seyfarth Kenya (1983)

C. sabaeus 56.3 Mixed St. Kitts, Caribbean Chapman & Fedigan (1984)

C. sabaeus 15.3 Mixed Barbados, West Africa Horrocks (1986)

C. aethiops 12.2 Savanna Amboseli National Park, Isbell (1990) Kenya

C. sabaeus 18 Mangrove Dania Beach, Florida Hyler (1995)

C. pygerythrus 24.5 Mixed Samara Game Preserve, Lucas (2014) South Africa

C. sabaeus 10.25 Mangrove Dania Beach, Florida Current study

The demographic composition and group size varied among the social groups (see

Table 6). Vervet social groups typically consist of 1 to 7 adult males and 2 to 10 adult females, with total group sizes ranging from 7 to 53 individuals (Cheney & Seyfarth,

1990; Struhsaker, 1967b). The size and composition of the largest groups, P1 and P2, remained relatively steady during the study period. Group P1 ranged in size from 12 to 19

(mean = 14 individuals; SD = 2.7). Group P2 ranged in size from 11 to 19 (mean = 15.6;

SD = 2.7) individuals. Group M3 ranged in size from 3 to 8 (mean = 6.4; SD = 1.7)

36 individuals and experienced a 63% decrease in size during the study period. Group M4 ranged in size from 1 to 2 individuals, both adults. In June 2014, group M4 consisted of two adult females living alone. From January 2015 to June 2016, group M4 consisted of only a single adult female. In January 2017, an adult male arrived and was observed with the lone adult female until the end of the study period. Among all four social groups, 74% of the adult animals were female (Altmann & Altmann, 1970).

Table 6

Demographics of the Social Groups 2014–2018

Group Sex & Age Jan. June Jan. June Jan. June Jan. June Jan. 2014 2014 2015 2015 2016 2016 2017 2017 2018 P1 Male 2 2 2 2 2 2 2 1 Female 2 2 2 2 5 5 5 5 Juvenile 7 7 7 8 4 4 4 9 Infant 1 1 1 1 1 5 5 4 Total 12 12 13 12 12 16 16 19 P2 Male 1 1 2 1 2 2 2 2 2 Female 5 6 6 6 6 6 6 6 6 Juvenile 4 3 3 5 5 7 7 8 7 Infant 1 2 3 3 6 4 1 1 2 Total 11 12 14 15 19 19 16 17 17 M3 Male 1 1 1 1 1 1 1 1 Female 2 2 2 2 2 2 2 2 Juvenile 3 3 3 5 4 1 1 0 Infant 1 2 1 0 1 1 1 0 Total 7 8 7 8 8 5 5 3 M4 Male 1 1 1 Female 2 1 1 1 1 1 1 1 Juvenile Infant Total 2 1 1 1 1 2 2 2

37 Births. Our results were consistent with those of other studies of vervet reproduction (Cheney et al., 1988; Fairbanks & McGuire, 1984; Horrocks, 1986; Isbell et al., 2009). Birth rates are limited by the number of breeding females (Horrocks, 1986).

Only 56% of the adult females gave birth annually. We recorded 35 births during the observation period. We identified the sex of 25 of the infants born (14 male, 11 female).

Seven of the infants died or disappeared before we could determine the sex, and the remaining three infants were difficult to observe. The mean number of offspring per female was 0.73 (SD = 0.31). Four of the females transitioned from juvenile to adult status during the study period and gave birth to their first infants during the last year of the study. One adult female did not give birth during the study period even though an adult male was present. Two females that were adults at the start of the study gave birth only once during the study period. Vervets decline in fecundity starting at 16 years of age, and we suspect that those two females were around that age or older based on their physical appearance (thin grey hair, thin body frame, heavy facial depigmentation, and slow crippled gait) (Atkins et al., 2014).

Of the 35 births, 91% (32) occurred between May and October, with a peak birth rate in July (see Figure 7). The seasonal increase in the birth rate coincided with the rainy season in south Florida (Pearson linear correlation, r = 0.6, p = 0.04). Other populations of vervets demonstrate birth seasonality as well (see Table 7). Seasonal births typically coincide with maximum food availability because of the energetic demands of lactation

(Horrocks, 1986). Of the 17 adult females, all but three gave birth during the study period, with a mean interbirth interval (IBI) of 12.9 (SD = 3.14) months. The longest and shorted IBI was 21.3 months and 8.2 months, respectively. We did not include the two

38 older adult females that only gave birth once in the IBI calculation. The IBI for the Dania

Beach population was comparable to that of wild vervets in Barbados (IBI = 11.8 months) and Segera Ranch, Kenya (IBI = 13.3 months).

Birth Distribution and Average Monthly Rainfall

14 12 12 10 10 8 8 6 6 4 4

2 2 in Inches Rain Total Total Number of of Births Number Total 0 0

Births Avg. rainfall

Figure 7. Birth distribution and average rainfall per month. The number of births (blue line) and the average rainfall (orange line) per month were assessed. There was a significant correlation between the number of births and average rainfall (Spearman’s rank correlation, r = 0.6, p = 0.04).

39 Table 7

Birth Seasonality Across Chlorocebus Populations

Births IBI Birth Season Avg. Infant Rainy Captive Location Author Mortality Season or Wild Rate

77 10.7 Peak in July, 13% died N/A C Sepulveda, Fairbanks & mos. year-round within one CA McGuire month; 6% (1984) died 1 mo.- 13 mo.

71 11.8 73% Apr.-Jul. 50% died Jun.-Nov. W Barbados, Horrocks mos. within first WI (1986) (n = 52) three years

86 17.1 87% Oct.-Dec. 57% Mar.-May W Amboseli Cheney et al. mos. National (1988) (n = 75) Nov.-Dec. Park, Kenya

58 13.3 *not described 48.3 %; 28 Mar.-May W Segera Isbell et al. mos. died before Ranch, (2009) Nov.-Dec. one year Kenya

35 12.9 91% May-Oct. 25% Jun.-Nov. W Dania Williams mos. Beach, FL (2018) (n = 32) Note. *Percentages represent the percentage of annual births that occurred during the birth season. Numbers in parentheses represent the total number of births that occurred during the birth season.

Mortality. A total of 22 individuals either died or disappeared during the study period (table in supplementary material). Most mortality occurred during the first year of life; 10 (29%) of the infants born during study period died before reaching 12 months of age. High infant mortality during the first year of life has been reported in both captive and free-ranging Old World monkeys (Cheney et al., 1988). The average annual infant mortality rate was 25% (SD = .11; see Table 8). The infant deaths were concentrated in the first 12 weeks of life (n = 9). The cause of infant mortality was difficult to determine because most (n = 6) of the infants that died disappeared overnight. Two infants were killed in accidents involving automobiles. One infant disappeared within 24 hours of

40 receiving a severe laceration of the right arm that caused profuse bleeding. One infant (<

2 weeks old) died of unknown causes and was carried by the mother for 24 hours after it died. Survivorship reached a steady state at 24 months of age (see Figure 8). This result is consistent with reports of other vervet populations, in which mortality is high during the first two years of life (Cheney et al., 1981).

Table 8

Annual Birth and Death Rates for Infants Born During Study Period

Birth Year Infants Born Infants Died Mortality Rate

2014 5 1 0.20

2015 9 1 0.05

2016 11 4 0.36

2017 10 4 0.40

Survival Rate 1.2 1 0.8 0.6 0.4

Percent Alive Percent 0.2 0 0 1 2 3 4

Age in Years

Figure 8. Kaplan-Meier survival (in years) of infants born during the study period.

Three adults and nine juveniles disappeared during the study period. The adult female that disappeared was reportedly hit by a car in Dania Beach. One adult male that disappeared seemed to be elderly with a slow arthritic gate, thin hair, and noticeable

41 weight loss. That individual suffered a traumatic wound prior to his disappearance, and we suspect that age and the severity of the wound contributed to his disappearance.

Another adult male died of electrocution while walking on power lines. The nine juveniles disappeared for unknown reasons.

Immigration and emigration. Vervet males typically transfer to neighboring social groups upon reaching sexual maturity (5 years of age) and then transfer to a new social group every 2–3 years thereafter (Cheney & Seyfarth, 1983). We documented 10 male dispersal events among the four social groups (see Figure 9). It was possible to document the origin and destination of eight of the male dispersal events because of the habituation of the animals and our familiarity with them. Five juvenile males (Abu, Scar,

Richard, Spike, and Juan) reached sexual maturity during the study and dispersed out of their natal groups. In June 2015, Abu left group P2 and immigrated into group P1. During that event, the resident adult male of group P1 (Alpha) left that group. Alpha was spotted in a residential community north of Port Everglades in August 2015 and was not seen again after that. Scar left group P2 in November 2015. A lone male monkey, possibly

Scar, was reported in a residential area south of WLP in the two months following Scar’s disappearance; however, no photos were taken to confirm its identity. An adult male of unknown origin (Mystery Man) immigrated into group P2 in January 2016. The resident male of group P2 (Mikey) left that group 11 months after the arrival of Mystery Man and immigrated into group M3, causing the M3 resident male (Tarzan) to emigrate out and move south across the Dania Beach Cut-off Canal to join a lone female. Richard emigrated out of group M3 when Mikey arrived and immigrated into group P2. Spike was observed in a residential neighborhood north of Port Everglades in November 2017.

42 Spike returned to Dania Beach and was documented in group P2 in April 2018. In

February 2018 another adult male, Goober, of unknown origin immigrated into group

M3, forcing the resident alpha male, Mikey, to emigrate out and return to group P2. Juan was last recorded with his social group in November of 2017 and was not observed since.

Figure 9. Recorded male emigration and immigration events during the study period 2014–2018. Names are abbreviated. Arrows indicate the direction of the dispersal event. Question marks indicate unknown origin or dispersal location.

Vortex models. All the model scenarios resulted in a decline in growth rate (stoc- r) for the population (see Table 9). The predicted final population size was close to the

SD of the population size in each scenario, indicating an unstable population (Stark et al.,

2012). The greatest average drop in population size came from scenario S5, which gave a

PE of 91% over the next 100 years. That scenario showed a TE of 52.33 (SD = 20.88) years and a mean population size of 22 (SD = 26.43) individuals after 100 years. Of the five scenarios, scenario S1 gave the average predicted population size (39 individuals, SD

= 33.47) that was closest to the measured population size in 2018 (41 individuals).

Scenario S1 included no harvest or additional social groups in the parameters and produced a PE of 9% for the 26 year timeframe (1992-2018). Scenario S4 gave a similar

43 prediction for final population size (34 individuals, SD = 33.73). Scenario S4 included an additional social group and an annual harvest. Scenarios S2 and S3 gave the smallest stoc-r [-0.05 (SD = 0.22) and -0.01 (SD = 0.21), respectively]. Interestingly, when the timeframe for S1 was changed to model hypothetical growth over a 100-year period based on Hyler’s data (1992-2092), the predicted extinction rate was 92% with a stoc-r [-

.05 (SD=.22).

The output results showed a reduction in the predicted extinction rate when the percentage of adult breeding females were increased by increments of 10%. The baseline model, S5, gave an extinction rate of 91% with a stoc-r [-.40 (SD = .22)] within the 100- year timeframe. The greatest reduction in the extinction rate was when the percent of adult breeding females was changed to 96%, the extinction rate was 1% with a stoc-r [-

.07 (SD = .22)]. The change in this parameter input suggests that the reproductive success of adult females is a key factor in the growth of the population.

Table 9

Results from Model Scenarios (1000 Iterations) for the Dania Beach Monkey Population

Scenario Scenario Initial N PE TE (SD) Det-r Stoc-r (SD) N-extant (SD) Timeframe

S1 1992-2018 36 .09 19.90 (5.14) .0087 -.016 (0.21) 39 (33.47)

S2 1992-2018 36 .30 20.03 (4.43) .0087 -.05 (0.22) 24 (27.27)

S3 1992-2018 48 .05 21.26 (4.30) .0087 -.01 (0.21) 51 (43.56)

S4 1992-2018 48 .17 20.73 (3.95) .0087 -.43 (0.21) 34 (33.73)

S5 2018-2119 41 .91 52.33 (20.88) .0087 -.40 (0.22) 22 (26.43) Note. Initial N: initial population size; PE: probability of extinction; TE: mean number of years to extinction; det-r: deterministic growth rate (mean growth rate from average birth and death rates; stoc-r: mean growth rate (mean stochastic population growth/decline rate), N-extant: mean number of individuals not extinct after time entered; SD: standard deviation.

44 Discussion

The introduced Dania Beach green monkey population has been living in Dania

Beach, Florida since the late 1940s when a small group of monkeys escaped from the

Dania Chimpanzee Farm. Our primary goals were to reassess the Dania Beach green monkey population’s demographics and analyze the viability of the population. We expected to find that there had been population growth and range expansion due to the adaptive nature of vervet monkeys, which tend to do well in human-disturbed habitats and have a generalist digestive system that allows them to survive on a variety of foods

(Chapman et al. 2016; Guy & Curnoe, 2013). Despite the population’s persistence, there has been very little growth. The population has grown only 13.8% since 1992, and distribution appears to be limited within the WLP boundaries. Because green monkeys are habitat generalists and opportunistic omnivores that thrive in agricultural and human- disturbed areas, the modest population growth was surprising (Boulton et al., 1996;

Brennan, 1985; Kavanagh, 1980). It is unlikely that the population is restricted by density because other Chlorocebus populations have been reported to have densities greater than

175 animals per km2 (Gartlan, 1969; Harrison, 1983). The underlying cause of the low rate of population growth is probably the scarcity of natural food sources in the mangroves and adjacent urban areas, as food availability strongly impacts reproduction and survival in nonhuman primates (Cheney et al., 1988).

Although vervets are opportunistic omnivores in most environments, it is possible that the homogenous mangrove habitat of WLP may not offer a sufficient supply of natural food resources for population growth. There are few invertebrates (insects and mangrove crabs) and vertebrates (lizards and birds) for the monkeys to consume. Red

45 mangroves and a small portion of invertebrates make up a substantial amount of the

Dania Beach monkeys’ diet, which is supplemented by some provisioning from humans

(Hyler, 1995). Green monkeys in Africa and the Caribbean often live close to agricultural areas where they raid crops, as they prefer fruits and vegetables to other foods (Boulton et al., 1996). The size of the introduced green monkey population on St. Kitts and Nevis is estimated to be 50,000 individuals (K. Dore, personal communication, April 17, 2018).

St. Kitts and Nevis are volcanic islands composed of various habitats including rainforest, evergreen forest, cloud forest, mangroves, shrubland, riparian forest, woodlands, agriculture, and urban areas (Horwith & Lindsay, 1999). The mosaic landscape allows for exploitation of various food items (particularly crop raiding), which has contributed to the growth of the monkey population (Boulton et al., 1996). The Dania Beach landscape is surrounded by developed cities, which offer little natural space and no access to agricultural areas, leaving only the mangroves as a refuge for the monkeys to forage for natural foods. The mangroves may not be an optimal habitat to sustain the population, so the monkeys consume other available vegetation (e.g., ornamental plants in parking lots) and human foods. Few mammals exclusively occupy mangroves due to extreme conditions few species can tolerate (Nowak, 2013). Primates typically use mangroves as a refuge and have access to other spaces to acquire food (e.g., agricultural areas, food markets, etc.) (Nowak, 2013). For example, the C. sabaeus population in Senegal occupied mangrove habitat; however, study groups ranged into agricultural area bordering the mangroves (Galat & Galat-Luong, 1976).

The Dania Beach green monkey population has historically received provisioning from the local human community, and this offers insight as to why the monkeys have

46 maintained a consistent presence near businesses where human foods are intentionally provided. Vervets prefer human food because it is typically nutritionally dense and requires less foraging (Sengupta, McConkey, & Radhakrishna, 2015). Primates that receive provisioning from humans tend to minimize their movements through the landscape to stay close to the known food source supplied by humans (Brennan, 1985;

Sengupta et al., 2015). The Dania Beach green monkeys, like other provisioned primates, have learned to associate humans with food. For example, provisioned long-tailed macaques (Macaca fascicularis) in Singapore are concentrated in human areas and have learned to link humans with food (Sha et al., 2009). The barbary macaques (Macaca sylavanus) in Gibraltar are concentrated around tourist sites where humans regularly offer food items (Unwin & Smith, 2010). Vervet monkeys (Cercopithecus aethiops) in

Amboseli National Park, Kenya, were permanent residents around a tourist lodge where provisioning and food raiding activities occurred (Brennan, 1985). Given that provisioned primates quickly learn to associate humans and human-occupied areas with food, it makes sense that the Dania Beach vervet monkeys maintain a presence near the businesses surrounding WLP.

The provisioned Dania Beach monkey population had a small mean group size, relatively low fecundity among adult females, and interbirth intervals that were comparable to those of unprovisioned vervet populations. For example, in Amboseli

National Park, Kenya, vervets that occupied a low-quality habitat (lack of food availability) had longer interbirth intervals and a smaller social group compared with vervets that occupied a high-quality habitat (Cheney et al., 1988). Provisioned primates typically have larger group sizes and shortened IBIs compared with unprovisioned

47 primates (Sengupta et al., 2015; Sha et al., 2009; Unwin & Smith, 2010). For instance, in the 1950s and 1960s the provisioned macaque (Macaca fuscata) population at

Takasakiyama, Oita Prefecture, Japan, grew too large for the natural area to sustain

(Kurita, Sugiyama, Ohsawa, Hamada, & Watanabe, 2008; Sugiyama, 2015). When wildlife managers reduced the amount of provisioned foods, the population size declined

(Kurita et al., 2008). In the vervet population in suburban KwaZulu-Natal, South Africa, larger social groups were documented near sites with provisioned food and access to water (Patterson et al., 2018). Vervets living in the urban areas of South Africa depend on provisioned food year-round (Patterson et al., 2018). It is reasonable to assume that the

Dania Beach green monkeys have learned to depend on foods provided by humans.

Based on the small group sizes and low fecundity of the adult females, we surmise that the rate of provisioning and quality of food items are unpredictable. Additionally, several businesses have implemented a no-feeding rule for employees.

The Vortex results suggest that the population is unstable and subject to extinction within the next 100 years. Both S1 and S5 predicted extinction with a mean of 49.4 years for time to extinction. The demographic data (births, mortality, interbirth intervals, group size, and social group structure) recorded in the Dania Beach monkey population follow other Chlorocebus populations. Even when trapping was removed from the modeling parameters, the predicted rate of extinction was above 90%. However, the predicted rate of extinction was positively impacted by changing the percent of breeding females. Just a

10% increase, reduced the predicted extinction rate significantly from 91% to 53%. It is unclear as to what is influencing the reproductive success of the adult females. Perhaps the homogenous mangrove habitat contributes to the reproductive success of the adult

48 females. Food supply affects fecundity, which can be measured through reproduction

(Cheney et al, 1988). Other vervet studies show that fecundity is reduced due to low quality habitat (minimal food and water available) (Cheney et al., 1988). Further analysis is needed to determine what factors are preventing the green monkey population from expanding as documented in other introduced adaptable primates (e.g., Silver Springs macaques and Caribbean green monkeys) (Anderson et al. 2017; Dore, 2013; Riley &

Wade, 2016).

49 CHAPTER 3. THE TOLERANCE, PROVISIONING, AND WOUNDS OF THE

DANIA BEACH MONKEY POPULATION

Introduction

Within the last century, human-wildlife interactions have increased due to urban development and will continue to intensify globally (Madden, 2004; Mormile & Hill,

2017; Patterson et al. 2018). These interactions can be positive, neutral, or negative depending upon the situation (Zulkifli, 2013). Typically, human-wildlife interactions are conflict-based due to an overlap of resources, such as food or space or wildlife activities negatively impacting human needs (Madden, 2004; Mormile & Hill, 2017). Factors such as cultural, financial, historical events, and health concerns make each conflict situation unique (Madden, 2004). Sometimes people report wildlife interactions to be beneficial to their well-being, while others report absolute intolerance (Patterson et al., 2017). The thoughts, actions, tolerance, and perceptions of the humans involved determine the outcome of these interactions and can provide insight for better understanding these wildlife interactions and mitigate human-wildlife conflict (Madden, 2004; Manfredo &

Dayer, 2004). Variation in tolerance is reported across stakeholders (Kansky, Kidd, &

Knight, 2016). The use of surveys in communities is a way to evaluate the attitudes and perceptions of the community and determine the extent of potential problems perceived by communities living in close proximity to wildlife (Kansky et al., 2016; Patterson et al.,

2017). The outcomes of such surveys can offer insights into the factors explaining tolerance. This provides a foundation to shape wildlife management programs and

50 increases the likelihood of such policies being accepted by the public (Kansky et al.,

2016; Patterson et al., 2017). Interactions between human and wildlife occur broadly across taxa, including mammals, birds, fish, reptiles, and insects (Manfredo & Dayer,

2004; Pimentel et al., 2005). In particular, the field of ethnoprimatology addresses the interface between human and nonhuman primate (Fuentes & Hockings, 2010; Hill &

Webber, 2010). Urbanization due to human activity has caused primate habitats to shrink and become more fragmented which leads to an increase in range overlap and competition for resources between humans and nonhuman primates (Fuentes &

Hockings, 2010; Lee, 2010; Mormile & Hill, 2017). These interactions can lead to interspecies conflict and possible disease transmission (Patterson et al., 2017). Few studies have focused on this human non-human primate interface within urban areas

(Mormile & Hill, 2017).

Several species of primates can co-exist with humans, including macaques

(Macaca spp.), baboons (Papio spp.), and vervets (Chlorocebus spp.). (Hill & Webber,

2010; Lee, 2010; Mormile & Hill, 2017; Patterson et al., 2018). These primates succeed in urban environments because they are behaviorally and ecologically flexible (Patterson et al., 2018). They are labeled as pests because they steal human foods from restaurants, garbage, hotels, homes, gardens, farms, and markets (Brennan, 1985; Else, 1991; Hill &

Webber, 2010; Mormile & Hill, 2017; Patterson et al., 2018). These highly desirable high-energy food items encourage the monkeys to maintain proximity to human areas only intensifying conflict (McKinney, 2011; Mormile & Hill, 2017). Food raiding behavior can result in the monkeys becoming the focus of lethal action by humans, such as poisoning, shooting, or trapping (Guy, 2013; Patterson et al., 2018). However, not all

51 human-nonhuman primate interactions are negative. In parts of Asia, primates, such as rhesus macaques (Macaca mulatta) and long-tailed macaques (Macaca fascicularis) have religious or spiritual value and are worshipped and provisioned in temples (Fuentes,

2010; Lee & Priston, 2005; Wolfe, 2002). These beliefs result in cultural norms that forbid the killing or injury of these animals (Hill & Webber, 2010; Lee & Priston, 2005).

Further, in many places, primates are kept as pets, trained for entertainment, or have become a focal point for ecotourism (Fuentes & Hockings, 2010).

The provisioning or deliberate feeding of primates by humans is common (Fa &

Southwick, 1988; Lee & Priston, 2005; Sengupta et al., 2015). Historically, long-term provisioning was used by researchers when habituating primates for observation (Fa &

Southwick, 1988). Present-day provisioning of primate populations is mostly a result of religion, tourism, wildlife management, and modified landscapes (Berman & Li, 2002;

Dubois & Fraser, 2013; Orams, 2002; Sengupta et al., 2015; Sengupta & Radhakrishna,

2018; Unwin & Smith, 2010). Some people seek out deliberate contact with monkeys and initiate interaction through feeding, seeing it as a positive experience (Lee & Priston,

2005; Sengupta & Radhakrishna, 2018). People want to “reconnect” with nature and view these close encounters as enriching (Orams, 2002). It is suggested that conservation campaigns and environmental-based media are spurring humans to seek ways to commune with nature in an effort to feel connected to these movements (Orams, 2002).

However, what is viewed by humans as a positive interaction, can result in negative consequences for the provisioned animals (Brennan, 1985; Dubois & Fraser, 2013; Else,

1991; Fa & Southwick, 1988; Lee & Priston, 2005; Mormile & Hill, 2017; Orams, 2002;

Saj, 1998).

52 Provisioned primates that view humans as a food source are at a greater risk of injury or death due to increased contact with humans and human technology. Human contact comes with dangers such as auto collisions, anthropozoonotic diseases, electrocution on high power voltage lines, retaliation from people, and lethal management of populations or individuals (Fuentes & Hockings, 2010; Guy, 2013;

Mormile & Hill, 2017; Patterson et al., 2018; Riley & Wade, 2016; Wallis & Lee, 1999).

Supplemental feeding can also cause an increase in intragroup aggression when food items due are clumped or temporally available (Altmann, 1988; Basckin & Krige, 1973;

Brennan, 1985; Gartlan, 1969; Orams, 2002; Saj, 1998; Unwin & Smith, 2010). Direct competition between conspecifics for access to provisioned food increases aggression rates (Basckin & Krige, 1973; Brennan, 1985; Gartlan, 1969; Saj, 1998; Unwin & Smith,

2010).

Competition for access to food resources can be divided into scramble and contest competition (Lal & Rajpurohit, 2010; Saj, 1998). Scramble competition is indirect, as resources are dispersed and food can be obtained nearly equally among social group members (Saj, 1998). Individuals avoid each other by spreading out to forage, which minimizes intragroup competition for food. In contest competition, individuals directly compete with each other for access to clumped resources and vary in the amounts of food acquired (Saj, 1998). Provisioned food is typically clumped in distribution, causing contest competition between individuals. Clumped foods are considered more usurpable than dispersed food and can increase intragroup aggression (Pruetz & Isbell, 2000). In natural settings, monkeys rarely feed in close proximity to one another (Brennan, 1985;

Pruetz & Isbell, 2000). Provisioning breaks down the socially prescribed distance, known

53 as the tolerant/intolerant distance (Furuichi, 1983), between individuals when feeding on human handouts, which leads to an increase in intragroup aggression (Brennan, 1985).

Agonism increases when an individual does not maintain this tolerant distance during feeding (Furuichi, 1983). Conversely, when human food is scattered widely over an area, aggression rates are lower since the monkeys can adequately maintain the socially acceptable distance within the group (Furuichi, 1983). The results of these agonistic bouts are a high rate of injuries, physical abnormalities, and permanent disfigurements (Basckin

& Krige, 1973; Brennan, 1985).

The present study focuses on the introduced green monkey (C. sabaeus) population (n = 39), that escaped from the Dania Chimpanzee Farm in the late 1940s in

Dania Beach, Florida. This commensal primate is considered a pest primate in its native

African range and on the Caribbean Islands of St. Kitts-Nevis and Barbados due to food raiding of public spaces and agricultural areas (Brennan, 1985; Dore, 2013; Patterson et al., 2018). Additionally, vervets in Africa, have displayed aggression towards humans after becoming accustomed to and expectant of food handouts directly from people

(Patterson et al., 2017). As a result, vervets are common in wildlife centers due to injuries received from humans due to pest behaviors (Patterson et al., 2017). In this study, I investigated the relationship between residents and monkeys in Dania Beach, Florida. An online survey was used to assess the community’s perceptions and opinions of the monkeys. This survey evaluated how the public felt about the presence of the monkeys in both residential and business locations. Also, I was interested in the type of interactions between humans and green monkeys. I observed and quantified the provisioning of the monkeys by the community over 12- month period. Further, I investigated the potential

54 impacts provisioning has on intragroup aggression through the observation and analysis of wounds. I predicted that the community would tolerate the monkeys and provisioning was reflective of a positive perception. I also predicted that due to provisioning, the population would demonstrate a higher number of wounds compared to non-provisioned monkey populations.

Methods

Survey data. An online anonymous survey was created on Survey Monkey to assess public opinion about the introduced green monkey population in Dania Beach,

Florida. The questionnaire was conducted from May 2015-June 2018. To reach a broad audience (to include individuals that did not know about the local monkey population), a link to the survey was available through the Dania Beach Vervet Project Facebook page

(referred to DBVP hereafter), the DBVP project website, included in local media coverage, educational talks presented to various community organizations, and DBVP flyers. The survey was composed of 39 questions that included both open-ended and fixed response questions (Bernard, 2006). The survey asked participants about: 1) attitudes towards nature, 2) attitudes towards the introduced monkey population, and 3) opinions about interactions between human and nonhuman primates. Demographic and socioeconomic variables were collected to include: 1) sex, 2) education level, and 3) household income. Additionally, participants were asked to list any environmental or animal welfare affiliations.

Survey data statistical analysis. Data were analyzed at the individual level expressed as a percentage of interviewees that gave a certain response (Nekaris, Boulton,

& Nijman, 2013). Non-parametric tests were used to investigate the demographic,

55 socioeconomic, and attituded variables that best explained the public’s attitudes, perceptions, and tolerance of the Dania Beach monkeys.

Provisioning data. Provisioning data were collected from January 2016-January

2017 at two known provisioning sites of the introduced African green monkeys (C. sabaeus) in Dania Beach, Florida. Individual monkeys (n = 39) were distinguished by facial markings, scars, missing limbs, and sex. I rotated site visits for a total of 158 times

(mean of 79 visits per site) from 8:00 a.m. to 5:00 p.m. for a combined total of 191 hours and 28 minutes of observation time (mean of 96 hours per site). The name of provisioners and locations are anonymous at the request of informants. Provisioning was defined as the intentional distribution of food items to the monkeys by humans. I recorded provisioning through: 1) direct observation, 2) informants, and 3) camera trap photos.

Direct observation occurred when a feeding event was witnessed. Informants were individuals who provisioned the monkeys and recorded provisioning events on a provided sheet that was collected weekly. Informants were regular provisioners that volunteered feeding information when I was not present to make observations. They recorded: 1) date, 2) time, 3) number of monkeys present, and 4) types of food provided.

Two camera traps were mounted in front of one provisioning area. The camera trap photos provided provisioning data when I was absent from site due to daily rotations.

Due to the highly varied number of provisioners at this site, a provided data sheet was not feasible.

For each directly observed provisioning event the following were recorded: 1) date; 2) start and stop time of feeding event; 3) food items distributed; 4) method in which food was distributed to monkeys (hand fed, scatter, cluster, or combination of

56 methods); 5) food rejected or consumed; and 6) if event was initiated by monkey or human (see Table 10). A provisioning start time was recorded when a provisioner presented food to the monkeys. The provisioning event time ended when the last monkey left the provisioning area. If monkeys returned to eat any leftover foods from a previous event, it was not included as a new feeding event. Food rejection was documented when a monkey did not eat the food item. Food consumption was recorded when a monkey put food item in mouth, chewed, and swallowed, or stuffed into cheek pouches. Human initiated provisioning was defined as human approaching the monkey with the intention of feeding monkeys. Monkey initiated provisioning was when a monkey approached a human (within 1 meter) to beg for food item. Begging was expressed in various ways by the monkeys:1) standing on hind legs while looking at food item, 2) tugging on pant leg of human, 3) sitting and staring at food item, and 4) standing on hind legs while reaching for food item. The frequency of begging behavior was not quantified as it was not part of the study. It was used as a behavioral cue to record provisioning.

Table 10

Provisioning Event Categories and Definitions

Provisioning Definition Category

Hand fed Human(s) feed monkey(s) directly from hand.

Scatter Human(s) distribute food over wide area to allow monkey(s) to feed self (> .5 meter). Food is on a substrate.

Cluster Human(s) provide food in a clustered area in which monkeys feed directly next to conspecific (< .5 meter). Food is on a substrate.

Informant and camera trap records documented: 1) date, 2) time of event, 3) and food items distributed. Camera trap provisioning events were recorded from two Spartan

57 3G wireless infrared all -weather trail cameras placed at a provisioning site for a total of

730 camera trap days. The cameras have a detection range of 100 feet, detection angle of

52 degrees, and one second trigger speed. One camera was placed .15 meters above ground on base of tree facing the provisioning area. The second camera was placed on adjacent fence 1 meter from tree facing the provisioning area, .15 meters above ground.

The two cameras allowed the entire provisioning area to be visible without any blind spots. The beginning of a provisioning event was recorded when a human presented food items to monkeys. The provisioning event terminated when the human was no longer visible on the camera distributing food items to the monkeys. A new provisioning event would start if a human presented food items on camera to monkeys after last recorded feeding event. Batteries and SD cards were monitored weekly.

Wound data. Wound data were collected opportunistically during site visits to record provisioning from January 2016 to January 2017 in Dania Beach, Florida. During an encounter with a social group, I scanned each individual in view for wounds. Each animal’s identity, wound location, and wound type were recorded. Additionally, a photo database was created of wounds. Precise wound recording was feasible due to habituation of monkeys. Wounds were defined as broken skin with visible blood or tissue, and included bone fractures (Arlet, Carey, & Molleman, 2009). Wounds were categorized into: 1) abrasions, 2) punctures, 3) lacerations, and 4) fractures (see Table 11) (Arlet et al., 2009; Whitten & Smith, 1984). Any wounds that changed (healing time, wound to scar) were excluded as fresh wounds during observations. Due to the habituation of the monkeys, it was feasible to discern any new wounds from previously recorded wounds on same body area. For example, if a wound was healing on reliable measure to confirm a

58 new wound observation on same body part. If a previously noted wound was reopened it was documented as a new wound.

Table 11

Wound Type Definitions by Severity

Wound Type Definition

Abrasion Scrape on surface of skin

Puncture Skin pierced by teeth, circular in shape

Laceration Deep tear in skin tissue

Fracture Bone noticeably displaced

Wound data statistical analysis. Wound frequencies were tabulated by age/sex class, wound location, and wound type. VassarStats: Website for Statistical Computation

(Lowry, 2019) was used to complete Chi-square analysis, with the p-value significance threshold set at .05.

Results

Survey data. A total of 234 surveys were completed during the study period (see

Table 12). Respondents were primarily White (75%) and female (70%). Most respondents were college educated: 1) graduated high school 7%; 2) some college 32%; and 3) college graduate and beyond 60%. Reported income varied: 1) $0-$49,999/yr.

19%; 2) $50,000- $99,999/yr. 29%; and 3) $100,000+/yr. 41%. Additionally, 52% were part of an animal welfare organization, while 48% belonged to an environmental or conservation organization, such as Defenders of Wildlife, Nature Conservancy, Audubon

Society, Manatee Education and Outreach Center, Friends of Secret Woods, and Save the

Chimps.

59 Table 12

Socioeconomic Profile of the 234 Survey Participants

Socioeconomic Groups Number Answered

Female 164

Male 65

Income $0-$49,999/yr. 45

Income $50,000-$99,999/yr. 67

Income $100,000+/yr. 96

White 175

Non-White 48

High School Education 16

Some College 74

College Graduate 140 Note. Some respondents skipped the questions that identified socioeconomic status.

Attitudes towards monkeys in community. The majority of respondents had a favorable view of the monkeys. When asked how the community viewed monkeys in their neighborhood, 70% reported that the monkeys were openly welcomed and 57% of the respondents stated that they “like” or “enjoy” seeing the monkeys in the neighborhood. Most respondents (85%) said they would do nothing if they saw a monkey in their yard. Only 7% cited a health concern in the comment section when asked to explain their response to seeing a monkey in their yard. Businesses expressed similar views, with 58% reporting that the monkeys were openly welcomed and that the monkeys were a “daily pleasure.” Most respondents (63%) stated that they “liked” or “enjoyed” seeing the monkeys at work; however, 25% were concerned that the monkeys could enter buildings or cars. There were no reports of aggression or property damage in the surveys.

60 Concern for local monkey conservation. Broad support for protection by the state was reported across all demographic bases (see Figure 10). In an open-ended question that asked participants if they thought that the monkeys should receive protected status, only 7% of the respondents replied “no,” citing concern for the non-native status of monkeys. The remaining 93% of the respondents conveyed that want the monkeys protected, used phrases such as “deserve protection,” “protect monkeys from humans,”

“loss of habitat,” “they are harmless,” and “human fault they are here” to explain their response.

Should the monkeys receive protected status from the state, county, or city? 100% 4 14 11 1000 8 4 10 10 7 6 95% 96 96 94 90% 92 93 89 90 90

Percent 85% 86 80%

75%

Demographic Groups

Yes No

Figure 10. Respondents in favor of changing law to protected status for the monkeys per demographic group.

A near unanimous opposition to removal of the monkeys was reported across all demographics (see Figure 11). In an open-ended question, only 9% responded that the monkeys should be removed from Dania Beach due to their nonnative status. The remaining 91% of respondents opposed removal, using phrases such as “they have a right

61 to be here,” “not a danger to anyone,” “let them be,” and “they have been part of Dania

Beach for years.”

Should the monkeys be removed? 100% 90% 80% 70% 60% 92 87 90 92 92 89 91 87 89 50% 93

Percent 40% 30% 20% 10% 8 13 10 8 8 11 9 13 11 0% 7

Demographic Groups

Yes No

Figure 11. Respondents against the removal of the monkeys per demographic group.

Provisioning the local monkey population. When asked if participants would feed the monkeys if it were the only way for the monkeys to survive, 58% reported yes

(see Figure 12). Of the 234 surveys, 9.5% (22 individuals) reported that they personally feed the monkeys. Of the 22 respondents that indicated they currently feed the monkeys, when asked if they will continue given the new law prohibiting feeding of wild monkeys in Florida, 50% reported that they will continue. In an open-ended question that asked these participants to explain why they fed the monkeys, phrases such as “deserve our help,” “they are family,” and “they need to survive” were given. 56% of these respondents reported that they provided food daily for the monkeys, 22% reported that

62 they feed the monkeys 2-4 times per week, and 22% reported that they feed the monkeys once a week.

Respondents Who Would Feed Monkeys for Their Survival if Needed

90% 75% 80% 80% 70% 57% 58% 60% 50% 36% 40% 30% 31% 30% 21% 20% Percent 20% 11% 10% 0%

Demographic Groups

Yes

Figure 12. Respondents who would feed the monkeys to survive per demographic group.

Provisioning data. A total of 427 provisioning events were recorded across the provisioning sites during the 12-month study period (see Figure 13). There was variation in the total amount of provisioning documented between the sites (see Table 13). The total is an estimate as it is likely that provisioning events were missed from: 1) random tourists and community members that fed opportunistically outside of observation times and camera traps, and 2) regular provisioners that did not participate as informants.

63 Provisional Events 250

200

150

Count 100

50 Total 0 Direct observation Reported Camera trap Provisioning Categories

Figure 13. Total provisioning events per category.

Table 13

Total Provisioning Events per Site

Provisioning Site Direct Observation Reported Camera Trap

Site 1 40 114 134

Site 2 38 101 * Note. *Camera trap not used at Site 2.

Of the 427 feeding events, 78 were directly observed. Directly observed feeding events captured the variation in how food was distributed. Hand fed provisioning was the most common type of feeding across all types of provisioning events (see Figure 14). Out of the 7 ways food was presented, 45% of the time food was distributed only by hand and

24% of the time the feeder also hand fed while scattering the food or putting food in a clump. The least common style of provisioning was the full combination of hand feeding, clustering, and scattering (1.3%). The mean provisioning event time was 7-8 minutes, with the shortest recorded at 5 seconds and the longest at 18 minutes. Shorter events occurred when a provisioner offered a food item and the monkey rejected the item (for example, cookies or bread that the monkeys find undesirable). The longest feeding events

64 occurred when the provisioner offered large quantities of food items that required processing by the monkey to eat (e.g., peanuts in a shell, bananas, or oranges).

Variation of Food Distribution to Monkeys by Humans 40 35 30 25 20 15

TotalCount 10 5 0

Feeding Style

Figure 14. Total counts of variation of food distribution styles to the monkeys by humans.

Of all recorded provisioning events (direct observation, informant, and camera trap), 50% of events occurred between 7:00 a.m. and 10:59 a.m., 34% of events occurred between 11:00 a.m. and 3:59 p.m., and 16% occurred after 4:00 p.m. The low number of reported evening events recorded after 4:00 p.m. may be attributed to the absence of informants in the late afternoon.

A variety of food items were offered to monkeys during the study (see Table 14).

The most common food items provided during provisioning events were bananas and nuts (peanuts in shell, salted peanuts, walnuts, and almonds). Bananas were offered 58% of the time and nuts offered 19.3% of the time. The remaining food items consisted of various fruits, root vegetables, candy, and packaged items. Food items consistently rejected when offered were lettuce, bread, shortbread cookies, dried tomato, and dragon fruit. 65 Table 14

Food Items Offered and Rejected During Study Period

Food Items Offered Food Items Rejected Apples Bread Bananas Dragon fruit Bread Dried tomatoes Candy (lemon heads, Snickers bars, Reese’s peanut butter cups, Lettuce M&Ms, Jolly Rancher hard candy, and peppermint balls) Cantaloupe Shortbread Cookies Carrots Cereal bars (strawberry and blueberry) Cherries Cookies (chocolate chip and shortbread) Dragon fruit Dried fruit (various types) Dried tomatoes Grapes Gum Lettuce Mango Mixed fruit bowl: melon, pineapple, and strawberries Nuts (various types) Oranges Papaya Plantain Rice Krispy Bars (regular and chocolate covered) Strawberries Trail mix

Wound data.

Wound distribution within age and sex classes. A total of 79 wounds were documented during the 12-month study period (monkeys were observed 127 times). An average of 6.58 wounds were recorded per month, with 47% (n = 37) occurring during

66 the rainy season months of June-November, which is also the birth season (see Figure

15). There was no correlation between total wounds per month and births (r = .21, p =

.26). However, there was a slight correlation between total wounds to adult females per month and births (r = .48, p = .06). This may be the result of higher resource competition during birth season due to increased energy requirements for lactation. Males received

75% (n = 18) of wounds between the months of December-May, which are associated with mating season. This pattern is comparable to other wild vervet populations where adult males receive most wounds during mating season (Freeman, 2012).

Wounds by Age/Sex Class 8 7 6 5

4 Wounds 3

Total 2 1 0

Month

AF AM Juv Infants

Figure 15. Observed monthly wounds during 12-month study period (January-December 2017) of age/sex classes. AF = adult female, AM = adult male, Juv = juvenile.

Age and sex were significantly associated with wounds. Adults (n = 58) received more wounds than juveniles (n = 16) and infants (n = 5) (휒 2 = 59.39, p = < .0001).

Females (n = 43, adults and juveniles) were wounded more often than males (n = 31, adults and juveniles) (휒 2 = 28.65, p = < .0001). Infant sexes (n = 5) were collapsed into one category due to low number of wounds per sex class. Adult and juvenile females 67 received more wounds than males. However, observed wounds were not distributed evenly across age classes. Interactions between age and sex were analyzed by further dividing the animals into adult males and females, juvenile males and females, and infants (sexes combined due to low number of wounds). Adult females received more wounds (43%) than all other groups, followed by adult males (30.4%), female juveniles

(11.4%), male juveniles (8.9%), and infants (6.3%) (휒 2 = 40.43, p < .0001) (see Table

15). This is unusual to other studies in which adult males were the recipients of most wounds (Baldellou, 1991; Basckin & Krige, 1973; Brennan, 1985; Freeman, 2012; Henzi

& Lucas, 1980; Lucas, 2014; Takahashi, 2012) (see Table 16). This suggests that the wounds were non-randomly distributed across age and sex classes. Overall adults received more wounds than juveniles and infants, with adult females recorded with most wounds.

Table 15

Total Observed Wounds per Age/Sex Class

Age/Sex Class Total Wounds Observed

Adult male 24

Adult female 34

Juvenile male 7

Juvenile female 9

Infants 5

68 Table 16

Comparative Wound Data Across Provisioned and Wild Vervet Populations

Species Total # Sex with Total Total Number Provisioned Author Wounds Most Observation of Individuals Wounds Time and Social Groups

C. aethiops 23 wounds/ Adult 120 hours 57 individuals Yes Basckin & scars males over 6 Krige 2 social months (1973) groups

C. aethiops 46 wounds Adult 12 months 89 individuals Yes Henzi & males Lucas 3 social (1980) groups

C. aethiops Not Not 500 hours Estimated 101 Yes Brennan quantified; quantifie over 5 individuals et. al noted high d months (1985) 4 social injuries or groups scars on all adults

C. pygerythrus 136 wounds Adult 1,192 hours 57 individuals Yes* Baldellou (88 wounds males over 2 years (1991) 3 social for captive groups group) (1 captive social group)

C. pygerythrus 46 wounds Adult 693 hours 121 No Freeman males over 9 individuals (2012) months 2 social groups

C. pygerythrus 110 wounds Adult 20 weeks 120 No Takahashi males individuals (2012) 2 social groups

C. pygerythrus 245 wounds Adult 9 months 53 individuals No Lucas females (2014) 2 social groups

C. sabaeus 79 wounds Adult 191 hours 41 Yes This study females over 12 individuals/4 months social groups Note. *One provisioned captive social group.

69 Wound type and location within age and sex classes. Wound types were nonrandom in distribution among age and sex classes. Lacerations (n = 61) were significantly more common (77.2%) than punctures (5.1%), abrasions (10.1%), and fractures (7.6%) (see Table 17). Overall, females (n = 38, juveniles and adults) received more lacerations than males (휒2 = 31.88, p = < .0001), with adult females receiving the most lacerations of any age or sex class (휒 2 = 47.11, p = < .0001). This is above the expected laceration count of 26.25 for adult females when compared to other age and sex classes (휒 2 = 9.8632, p = .042796, p < .05) (see Table 18). Adult females (n = 4) also received 80% of the puncture wounds (n = 5). Adult males received 50% of the total documented fractures (n = 6) and 50% of the total noted abrasions (n = 8).

Table 17

Total Wound Type per Age/Sex Class

Age/Sex Class Abrasion Laceration Fracture Puncture

Adult male 4 17 3 0

Adult female 0 31 0 3

Juvenile male 0 4 2 1

Juvenile female 1 7 1 0

Infants 3 2 0 0

Total 8 61 6 4

70 Table 18

Expected and Observed Wound Type per Age/Sex Class

Age/Sex Class Laceration Abrasion/Fracture/Puncture*

Expected Observed Expected Observed

Adult male 18.53 17 5.47 7

Adult female 26.25 31 7.75 3

Juvenile male 5.41 4 1.59 3

Juvenile female 6.95 7 2.05 2

Infants 3.86 2 1.14 3 Note. *The abrasion, fracture, and puncture categories were collapsed due to 0 values.

At the population level, the location of wounds on the body were randomly distributed, apart from the back/chest/abdomen area (see Table 19) (휒 2 = 6.38, p = .17).

However, there were differences in the number of wounds per body part within age and sex classes (휒 2 = 23.13, p = .03) (see Table 20). Specifically, when adult sex classes were compared results showed that adult males received a disproportionately highly number of wounds on the head and arms, while adult females received more wounds on the legs and tail (휒 2 = 14.0974, p = .006991, p < .05) (see Figure 16). These findings are consistent with other vervet populations with males receiving most wounds to the head area and forelimbs (Freeman, 2012; Lucas, 2014; Takahashi, 2012). Adult males received a total of 17 wounds between the head (n = 10) and arms (n = 7), while females received only four wounds on the head and four wounds on the arms. Adult females received a total of

23 wounds between the legs (n = 15) and tail (n = 8), while adult males received only four wounds on the thighs and one wound on the tail. There was no significant difference between adult males and females in the number of wounds recorded on the back/chest/abdomen area (adult males, n = 2; adult females, n = 3). 71 Table 19

Total Wounds on Body Location per Age/Sex Class

Age/Sex Class Head Arms Legs Tail Back/Chest/Abdomen

Adult male 10 7 4 1 2

Adult female 4 4 15 8 3

Juvenile male 0 2 2 2 1

Juvenile female 1 3 0 4 1

Infants (male and female) 1 1 1 1 1

Total 16 17 22 16 8

Table 20

Expected and Observed Distribution of Wounds on Body Parts by Age/Sex Class

Age/Sex Class Head Arms Legs Tails Back/Chest/ Abdomen

Exp. Obs. Exp. Obs. Exp. Obs. Exp. Obs. Exp. Obs.

Adult male 4.86 10 5.16 7 6.68 4 4.86 1 2.43 2

Adult female 6.89 4 7.32 4 9.47 15 6.89 8 3.44 3

Juveniles 3.24 1 3.44 5 4.46 2 3.24 6 1.62 2 (male and female)

Infant (male 1.01 1 1.08 1 1.39 1 1.01 1 0.51 1 and female)

72

Figure 16. Distribution of total wounds by body part for adult males and adult females. Observed wounds are listed first and expected wounds are in parentheses. *Denotes body parts that received more wounds than expected.

73 Discussion

Public perceptions, attitudes, and provisioning. This was the first comprehensive public survey to look at the local attitudes and perceptions of the green monkeys of Dania Beach, Florida. People that live and work alongside commensal primates typically report them as a threat or a pest (Hill, 2004). However, this was not found in the respondents of this survey. Most of the community reported positive attitudes towards the monkey with widespread local support for their protection and welfare. This is unusual since Chlorocebus monkeys normally are reported as nuisances in Africa and the Caribbean (Brennan, 1985; Chapman et al., 2016; Dore, 2013; Patterson et al., 2018; Saj, 1998). There are several factors that may influence the attitude of the local community.

The concern for animal welfare and wildlife conservation and environmentally based media, contributes to an increasing tolerance and appreciation of wildlife (George,

Slagle, Wilson, Moeller, & Bruskotter, 2016; Orams, 2002). Most of respondents in this survey reported a positive perception regardless of whether the monkeys visited their neighborhoods or businesses. Some of the respondents were not even aware of the monkey population in Florida and still reported a positive reaction. The common denominator was the concern overall for animal welfare and/or wildlife conservation.

Many respondents belonged to animal welfare groups and/or wildlife conservation groups. Other studies assessing wildlife tolerance reported similar findings (Nekaris et al., 2013; Patterson et al., 2017). Many survey participants gave conservation or welfare- based statements in open ended questions using phrases such as “loss of habitat,”

“humans are responsible for their protection,” and “they deserve to be here.” These

74 statements reflect wild life values of mutualism and environmentalism (Dayer,

Stinchfield, & Manfredo, 2007). These pro-conservation/welfare sentiments were also documented in primate studies in Tanzania, South Africa, and Belize (Nekaris et al.,

2013; Patterson et al., 2017).

Wildlife tolerance occurs when there is minimal economic loss and minimal human health concerns (Patterson et al., 2017; Saj, 1998). The results of the public survey reported no personal or business damage and zero reports of aggression. This can be contributed to the location of the monkey population in Dania Beach. The monkeys occupy mangrove habitat that buffers up against industrial areas (warehouses and parking lots) that are devoid of any natural food items apart from a few decorative plants placed by business management. Business employees keep their car windows rolled up, which reduces the possibility of monkeys entering a vehicle to search for any possible food items. The opportunities for the monkeys to display any pest like behaviors are greatly minimized because of this environment, thus no reported economic loss or damage.

Because of this, employees reported the monkeys as a “daily pleasure” and “harmless” with no reports of aggression or safety concerns. There have been confirmed reports of dispersing males entering neighborhoods. However, the community offered food items to the animal and feared for the safety of the monkey. People enjoyed seeing the monkey in their neighborhood, with few expressing concerns for human safety. This tolerant attitude can be attributed to a novel experience that is absent of negative historical interactions with monkeys. A survey completed on urban vervets in South Africa reported a similar response in which respondents reported a positive opinion of the monkeys when food

75 raiding was absent, health concerns were minimal, and reported aggression was low

(Patterson et al., 2017).

When feeding wildlife there are inherent risks for both animal and human (Orams,

2002). However, research suggests that people acquire some psychological satisfaction in provisioning of wildlife (Lee & Priston, 2005; Orams, 2002). Primates are one of those animal species that people feel connected to and provision for various reasons (religious, cultural, or personal purposes) (Nekaris et al., 2013; Sengupta & Radhakrishna, 2018).

The survey showed that the community of Dania Beach is no exception. Individuals purposely purchased food to provision the monkeys and many of the interactions resulted in food being handed directly to the animals. Many respondents stated that they fed the monkeys because “they are family.” Many survey participants also said they will continue to provision regardless of laws against feeding wild monkeys in Florida. This, like in other studies, demonstrates that people feed the animals to show tolerance towards them, enjoy the interaction, and will continue to feed despite any laws that may prohibit provisioning (Orams, 2002; Sengupta & Radhakrishna, 2018). However, this interaction creates a cycle of dependence on human for food, as the monkeys become accustomed to provisioning and actually prefer human foods over natural food items (Lee & Priston,

2005). This leads to habituation to people and causes the monkeys to seek out food items on parking lots where provisioning regularly occurs. Since the monkeys are openly welcomed, this food seeking behavior is rewarded through provisioning. This case of primate tolerance can contribute to better understanding the motivations of human- wildlife relationships and interactions, and help shape conservation movements, wildlife management, and mitigate conflict in other settings.

76 Wounds. Wounds are proxies of severe aggression due to provisioning (Freeman,

2012; Lal & Rajpurohit, 2010; Self et al., 2013). The free-ranging green monkeys observed in this study displayed a high number of wounds compared to other free ranging provisioned vervet populations. Provisioned food occurred at high concentrations over limited areas. The frequency of agonistic interactions is expected to increase as items become more usurpable (Isbell & Pruetz, 1998). Also, the clumped distribution of provisioned food items reduces conspecific proximity. Of the observed feeding events,

80% involved some form of cluster feeding or hand feeding. Additionally, during hand feeding events, food was distributed to individual monkeys one at a time. Certain monkeys were fed first simply because the provisioner had a “favorite.” This preferential feeding inadvertently disrupted the hierarchy, allowing potentially lower ranking individuals access to a highly desirable food item over higher ranking individuals. It is possible that the direct hand feeding of individual monkeys contributed to the observed wounds, driving punishment actions within the social groups. Other studies have documented punishment in vervets, macaques, and mandrills (Arseneau-Robar, Taucher,

Schnider, van Schaik, & Willems, 2017; Chancellor & Isbell, 2008; Lucas, 2014; Schino

& Marini, 2014).

This study shows that total wounds received was greater for adults, specifically females, than for any other age or sex class. The differences in wound location and number between adult males and females can be attributed to variation in the competition for resources (mating and food) (Archie, Altmann, & Alberts, 2014). Adult male vervets typically engage in agonistic bouts face to face, which leads to an increase in head and arms wounds (Baldellou, 1991; Takahashi, 2008; Whitten & Smith, 1984). Although

77 wounds in adult males were recorded year-round, most of the wounds occurred during dispersal events before the onset of birth season in May, with most wounds recorded on the head and arms. This pattern was also observed in adult males in other studies during mating season (Freeman, 2012; Henzi & Lucas, 1980). Adult females received the majority of wounds on legs and tails. Adult females often fight by running and chasing, which accounts for wounds on tails and legs (Arlet et al., 2009; Whitten & Smith, 1984).

This wounding pattern may be attributed to intense provisioning leading to feeding competition. Although dominance ranking was not studied, it is possible that most of the adult females that were observed with wounds were lower ranking. Other studies have documented more wounds in lower ranking individuals in provisioned monkey populations (Lal & Rajpurohit, 2010). This study noted wounds year-round in adult females, with peaks occurring during the birth season (May-October). Studies have noted that during pregnancy and lactation, female primates consume more food and seek out more densely nutritional food (Archie et al, 2014). The wounds observed in the adult females during the birth season may correlate to an increase in competition among individuals for human foods to accommodate the energetic demands of lactation. Long- term annual observations are needed to determine if there is a clear link between birth season, female wounds, and provisioning.

78 CONCLUSION

The green monkey (C. sabaeus) population in Dania Beach is unusual in various way when compared to endemic and introduced populations. The lack of population growth in Dania Beach, Florida is surprising considering this population: 1) is provisioned, 2) lacks evidence for regular trapping, and 3) has minimal predation pressures (Anderson, 2016). This species can increase in density in human modified landscapes where both natural and human provided foods are available (e.g., Caribbean population) (Brennan, 1985; Patterson et al., 2018; Saj, 1998). Additionally, the lack of growth is unlikely hindered by density as the vervet monkey population on the island of

St. Kitts (69 square miles) is estimated to be 434 km2 (Turner et al., 2016). It is possible due to a small founding population and small population size that gene flow is limited between social groups which may result in reduced genetic variability and inbreeding depression within groups (Richardson, 1990). Ongoing research currently researching the possible factors inhibiting expected population growth.

The public support and tolerance across all demographic groups is broad. This is unusual considering this type of primate is considered a pest in Africa and the Caribbean

(Brennan, 1985; Dore, 2013; Patterson et al., 2018). The factors influencing the positive attitude stems from the community’s opinions about wildlife conservation and animal welfare. Additionally, the public has reported zero incidents of aggression or property damage. Also, the monkeys have maintained a small population and home range within the mangroves that border industrial areas, only visiting adjacent business parking lots to

79 receive human provided foods. There are few reports of monkey sightings in residential areas. The combination of these factors minimized the opportunity for the monkeys to display typical pest like behaviors associated with this genus, contributing to the public support.

Due to the overwhelming public support, it is not surprising that people feed the monkeys. Many reported that they enjoyed the interactions and felt connected to the animals. This psychological satisfaction associated with feeding wildlife is common

(Dubois & Fraser, 2013). However, the negative impacts of provisioning in the Dania

Beach monkeys resulted in an increase in wounds due to feeding competition between individuals. Although the FWC passed a law stating that is illegal to feed wild monkeys, people continue to feed. The law is difficult to enforce as feeding is random. A public education campaign is a possible solution to minimize feeding by educating the public on the hazards of feeding wildlife. Apart from the wounds, provisioning promotes proximity between humans and monkeys, which is a potential health risk to both species.

The risk of disease transmission is low, as most vervets are disease free, and the few documented cases of disease transmission involved the butchering and hunting of monkeys or direct contact in a laboratory setting (Jasinska et al., 2013; Legesse & Erko,

2004; Wolfe et al., 2004). Caribbean green monkeys are free of many of the pathogens associated with other primates; including hepatitis A and B viruses, simian hemorrhagic fever virus, filoviruses, poxviruses, simian immunodeficiency virus (SIV), simian T- lymphotropic virus, simian virus 40, and yellow fever virus; because of their isolation from their African counterparts (Baulu, Evans, & Sutton, 2002; Fox, Otto, & Colby,

2015). The risk of SIV or SFV transmission is minimal in Dania Beach because the

80 monkeys are not hunted for food and have been isolated from African populations for 80 years. Also, it is possible for humans to transmit disease to animals (reverse zoonosis)

(Messenger, Barnes, & Gray, 2014). There have been documented cases of disease transmission (measles virus; influenza A virus; parainfluenza viruses 1, 2, and 3; and other contagious respiratory viruses) from humans to macaques, chimpanzees, and vervets (Gaetano et al., 2014; Jones-Engel, Engel, Schillaci, Babo, & Froehlich, 2001;

Messenger et al., 2014; Riley & Wade, 2016). There should be signs in places of known provisioning spots to make the public aware of the possible health risks of feeding the monkeys and how interactions with humans can alter the health and behavior of the animals.

The monkeys are a charismatic species which garner public support and can make any perceived invasive management difficult (Verbrugge, Van den Born, & Lenders,

2013). Currently there is no need to consider culling the population because research suggests that this population will not grow or spread outside of the Dania Beach area which reduces the need for any management intervention. This population offers unique opportunities to research a near threatened species in a novel habitat with unusual public support. The Dania Beach monkeys can provide insight to management and conservation efforts abroad.

81 APPENDIX

82 Appendix A. Mortality Table

Name Sex Social Age at Death / Date of Death or Disappearance Illness Confirmed Suspected Cause Group Disappearance Disappearance Death Predation Dot F M4 > 10 years 6/1/2014 x ? Gizmo F M3 11.8 months 6/10/2015 x Car Kinkerbell F P1 3.5 years 2/7/2016 x ? Hope ? P2 3 weeks 6/16/2016 x ? 2A ? P2 2.1 weeks 8/19/2016 x ? 3A ? P2 3 weeks 9/9/2016 x ? 1A ? P1 7 weeks 9/26/2015 x Hawk Grandpa M P1 > 15 years 10/5/2016 x Traumatic wound prior to disappearance Dexter F M3 1.8 years 10/11/2016 x ?

8 Swiper M M3 2.5 years 10/11/2016 x ?

3 83 Flower F P2 1.2 years 10/26/2016 x ? Cookie M P2 2.2 months 11/21/2016 x Car Monster Cinder M P2 1.6 years 1/31/2017 x ? 5A ? P2 0 weeks 6/20/2017 x ? Hershey ? P2 2 weeks 7/17/2017 x Unknown, mother carried dead infant for 24 hours Tucker M P2 1.6 years 8/19/2017 x ? Scooter F M3 1.2 years 10/1/2017 x ? Summer ? M3 1.1 months 10/21/2017 x ? 4A ? P2 1.2 months 11/15/2017 x ? Ace M M3 3.5 years 12/1/2017 x ? Mystery Man M P2 7 years 3/6/2018 x Electrocution Kip F M3 1.1 years 10/11/2018 x ? Total 16 1 4 1

REFERENCES

Altmann, J. (1988). Foreword. In J. E. Fa & C. H. Southwick (Eds.), Ecology and

behavior of food-enhance primate groups (pp. ix–xiii). New York, NY: Alan R.

Liss, Inc.

Altmann, S. A., & Altmann, J. A. (1970). Baboon ecology: African field research.

Chicago, IL: University of Chicago Press.

Anderson, C. J. (2016). Ecology and impacts of introduced non-human primate

populations in Florida (Doctoral dissertation). University of Florida, Gainesville.

Anderson, C. J., Hostetler, M. E., & Johnson, S. A. (2017). History and status of

introduced non-human primate populations in Florida, U.S.A. Southeastern

Naturalist, 16(1), 19–36.

Archie, E. A., Altmann, J., & Alberts, S. C. (2014). Costs of reproduction in a long-lived

female primate: Injury risk and wound healing. Behavioral Ecology and

Sociobiology, 68(7), 1183–1193. http://doi.org/10.1007/s00265-014-1729-4

Arlet, M. E., Carey, J. R., & Molleman, F. (2009). Species, age and sex differences in

type and frequencies of injuries and impairments among four arboreal primate

species in Kibale National Park, Uganda. Primates, 50(1), 65–73.

http://doi.org/10.1007/s10329-008-0119-9

Arseneau-Robar, T. J. M., Taucher, A. L., Schnider, A. B., van Schaik, C. P., & Willems,

E. P. (2017). The costs and benefits of female participation in between-group

84 conflicts in vervet monkeys. Animal Behaviour, 123, 129–137.

http://doi.org/10.1016/j.anbehav.2016.10.034

Atkins, H. M., Willson, C. J., Silverstein, M., Jorgensen, M., Floyd, E., Kaplan, J. R., &

Appt, S. E. (2014). Characterization of ovarian aging and reproductive senescence

in vervet monkeys (chlorocebus aethiops sabaeus). Comparative Medicine, 64(1),

55–62.

Avise, J. C. (2004). Molecular markers, natural history, and evolution (2nd ed.).

Sunderland, MA: Sinauer Associates, Inc.

Avise, J. C. (2009). Phylogeography: Retrospect and prospect. Journal of Biogeography,

36(1), 3–15. https://doi.org/10.1111/j.1365-2699.2008.02032.x

Baldellou, M. I. (1991). Implications of the multi-male troop structure in vervet monkeys

(cercopithecus aethiops pygerythrus) (Doctoral dissertation). University of

Kwazulu-Natal, Durban, South Africa.

Banker, D. (1991, October 31). Monkey researcher lingers in the swamp. South Florida

Sun Sentinel, p. 1B.

Barrett, A. S. (2005). Foraging ecology of the vervet monkey (chlorocebus aethiops) in

mixed lowlevel bushveld and sour lowveld bushveld of the Blydeberg

Conservancy, Northern Province, South Africa (Master’s thesis). Univeristy of

South Africa, Pretoria.

Basckin, D. R., & Krige, P. D. (1973). Some preliminary observations of the behaviour of

an urban troop of vervet monkeys (Cercopithecus aethiops) during the birth

season. Journal of Arid Environments, 1(5), 287–296.

85 Baulu, J., Evans, G., & Sutton, C. (2002). Pathogenic agents found in Barbados

Chlorocebus aethiops sabaeus and in Old World Monkeys commonly used in

biomedical research. Laboratory Primate Newsletter, 41, 4–6.

Berman, C. M., & Li, J. H. (2002). Impact of translocation, provisioning and range

restriction on a group of Macaca thibetana. International Journal of Primatology,

23(2), 383–397. http://doi.org/10.1023/A:1013891730061

Bernard, H. R. (2006). Research methods in anthropology: Qualitative and quantitative

approaches (4th ed.). Lanham, MD: Altamira Press.

Boulton, A. M., Horrocks, J. A., & Baulu, J. (1996). The Barbados vervet monkey

(Cercopithecus aethiops sabaens): Changes in population size and crop damage,

1980–1994. International Journal of Primatology, 17(5), 831–844.

https://doi.org/10.1007/BF02735267

Brennan, E. J. (1985). Ecology and behaviour of a pest primate: Vervet monkeys in a

tourist-lodge habitat. African Journal of Ecology, 23(1), 35–44.

Broward County Government. (2018). West Lake Park, Dania Beach, Florida [Map]. Ft.

Lauderdale, FL: Author.

Broward County Government. (2019). Anne Kolb Nature Center. Retrieved from

http://www.broward.org/Parks/Pages/Park.aspx?=1

Chancellor, R. L., & Isbell, L. A. (2008). Punishment and competition over food in

captive rhesus macaques, Macaca mulatta. Animal Behaviour, 75(6), 1939–1947.

http://doi.org/10.1016/j.anbehav.2007.11.007

Chapman, C. A., & Fedigan, L. M. (1984). Territoriality in the St. Kitts Vervet,

Cercopithecus aethiops. Journal of Human Evolution, 13(8), 677–686.

86 Chapman, C. A., Twinomugisha, D., Teichroeb, J. A., Valenta, K., Sengupta, R., Sarkar,

D., & Rothman, J. M. (2016). How do primates survive among humans?

Mechanisms employed by vervet monkeys at Lake Nabugabo, Uganda. In M.

Waller (Ed.), Ethnoprimatology, developments in primatology: Progress and

prospects (pp. 77–94). New York, NY: Springer.

Chauhan, A., & Pirta, R. S. (2010). Public opinion regarding human-monkey conflict in

Shimla, Himachal Pradesh. Journal of Human Ecology, 30(2), 105–109.

http://doi.org/10.1080/09709274.2010.11906279

Cheney, D. L., Lee, P. C., & Seyfarth, R. M. (1981). Behavioral correlates of non-random

mortality among free-ranging female vervet monkeys. Behavioral Ecology and

Sociobiology, 9(2), 153–161. https://doi.org/10.1007/BF00293587

Cheney, D. L., & Seyfarth, R. M. (1983). Nonrandom dispersal in free-ranging vervet

monkeys: Social and genetic consequences. The American Naturalist, 122(3),

392–412. https://doi.org/10.1086/284142

Cheney, D. L., & Seyfarth, R. M. (1990). How Monkeys See the World: Inside the Mind

of Another Species. University of Chicago Press.

Cheney, D. L., Seyfarth, R. M., Andelman, S. J., & Lee, P. C. (1988). Reproductive

success in vervets. In T. H. Clutton-Brock (Ed.), Reproductive success: Studies of

individual variation in contrasting breeding systems (pp. 384–402). Chicago, IL:

University of Chicago Press.

Colautti, R. I., & MacIsaac, H. J. (2004). A neutral terminology to define “invasive”

species. Diversity and Distributions, 10(2), 135–141.

http://doi.org/10.1111/j.1366-9516.2004.00061.x

87 Coleman, B. T., & Hill, A. (2015). Biogeographic variation in the diet and behaviour of

Cercopithecus mitis. Folia Primatol (Basel), 35(5), 319–334.

doi:10.1159/000368895

Cramer, J. D., Gaetano, T., Gray, J. P., Grobler, P., Lorenz, J. G., Freimer, N.

B.,…Turner, T. R. (2013). Variation in scrotal color among widely distributed

vervet monkey populations (Chlorocebus Aethiops Pygerythrus and Chlorocebus

Aethiops Sabaeus). American Journal of Primatology, 75(7), 752–762.

https://doi.org/10.1002/ajp.22156

Cunningham, D. (2011). Sight-seeing boats in mid-twentieth century Broward County.

Broward Legacy, 31(1), 41–53.

Dayer, A. A., Stinchfield, H. M., & Manfredo, M. J. (2007). Stories about wildlife:

Developing an instrument for identifying wildlife value orientations cross-

culturally. Human Dimensions of Wildlife: An International Journal, 12(5), 307–

315. https://doi.org/10.1080/10871200701555410

Decker, D. J., Gavin, T. A., & Greer, K. (2013). Public attitudes toward a suburban deer

herd. Wildlife Society Bulletin, 15(2), 173–180.

Dorcas, M. E., Willson, J. D., Reed, R. N., Snow, R. W., Rochford, M. R., Miller, M. A.,

…Hart, K. M. (2012). Severe mammal declines coincide with proliferation of

invasive Burmese pythons in Everglades National Park. Proceedings of the

National Academy of Sciences, 109(7), 2418–2422.

http://doi.org/10.1073/PNAS.1115226109

88 Dore, K. (2013). An anthropological investigation of the dynamic human-vervet monkey

(Chlorocebus aethiops sabaeus) Interface in St. Kitts, West Indies (Doctoral

dissertation). University of Wisconsin, Milwaukee.

Dore, K. (2017). Ethnophoresy. In A. Fuentes (Ed.), The International Encyclopedia of

Primatology (pp. 1–7). Cambridge, MA: Wiley-Blackwell.

Dorst, J. (1970). A field guide to larger mammals of Africa. Boston, MA: Houghton

Mifflin Company.

Dubois, S., & Fraser, D. (2013). A framework to evaluate wildlife feeding in research,

wildlife management, tourism and recreation. Animals, 3(4), 978–994.

http://doi.org/10.3390/ani3040978

Dunbar, R. I. M. (1974). Observations on the ecology and social organization of the

green monkey, Cercopithecus sabaeus, in Senegal. Primates, 15(4), 341–350.

https://doi.org/10.1007/BF01791671

Else, J. G. (1991). Nonhuman primates as pest. In H. O. Box (Ed.), Primate responses to

environmental change (pp. 115–165). London, United Kingdom: Chapman and

Hall.

Fa, J. E., & Southwick, C. H. (1988). Introduction. In J. E. Fa & C. H. Southwick (Eds.),

Ecology and behavior of food-enhance primate groups (pp. xv–xvii). New York,

NY: Alan R. Liss, Inc.

Fairbanks, L. A., & McGuire, M. T. (1984). Determinants and fecundity and reproductive

success in captive vervet monkeys. American Journal of Primatology, 7(1), 27–

38. https://doi.org/10.1002/ajp.1350070106

89 Fleshler, D. (2015, August 23). Dania Beach mangroves full of monkey business. South

Florida Sun Sentinel, pp. A1, A14.

Florida Fish and Wildlife Conservation Commission. (2019). Nonnative mammals.

Retrieved from http://myfwc.com/wildlifehabitats/nonnatives/mammals/

Fox, J. G., Otto, G. M., & Colby, L. (2015). Selected zoonoses. In J. G. Fox, L. C.

Anderson, G. M. Otto, K. R. Pritchett-Corning, & M. T. Whary (Eds.),

Laboratory animal medicine (3rd ed.) (pp. 1313–1370). Cambridge, MA:

Academic Press.

Freeman, N. J. (2012). Some aspects of male vervet monkey behaviour (Master’s thesis).

University of Lethbridge, Alberta, Canada.

Fuentes, A. (2010). Naturalcultural encounters in Bali: Monkeys, temples, tourists, and

ethnoprimatology. Cultural Anthropology, 25(4), 600–624.

http://doi.org/10.1111/j.1548-1360.2010.01071.x

Fuentes, A., & Hockings, K. J. (2010). The ethnoprimatological approach in primatology.

American Journal of Primatology, 72(10), 841–847.

http://doi.org/10.1002/ajp.20844

Furuichi, T. (1983). Interindividual distances and influence of dominance on feeding in a

natural Japanese macaque troop. Primates, 24(4), 445–455.

https://doi.org/10.1007/BF02381678

Gaetano, T. J. (2012). Hormonal and morphological aspects of growth and sexual

maturation in wild-caught male vervet monkeys (chlorocebus aethiops

pygerythrus) (Master’s thesis). University of Wisconsin, Milwaukee.

90 Gaetano, T. J., Danzy Cramer, J., Mtshali, M. S., Theron, N., Schmitt, C. A., Grobler, J.

P.,…Turner, T. R. (2014). Mapping correlates of parasitism in wild South African

vervet monkeys (Chlorocebus aethiops). South African Journal of Wildlife

Research, 44(1), 56–70. http://doi.org/10.3957/056.044.0105

Galat, G., & Galat-Luong, A. (1976). La colonisation de la mangrove par Cercopithecus

aethiops sabaeus au Senegal. La Terrer et La Vie: Revue d’Ecologie Appliquee,

30, 3–30.

Gartlan, J. S. (1969). Sexual and maternal behaviour of the vervet monkeys,

(Cercopithecus aethiops). Journal of Reproductive Fertility, Supplement 6, 137–

150.

George, K. A., Slagle, K. M., Wilson, R. S., Moeller, S. J., & Bruskotter, J. T. (2016).

Changes in attitudes toward animals in the United States from 1978 to 2014.

Biological Conservation, 201, 237–242.

http://doi.org/10.1016/j.biocon.2016.07.013

Gonedelé Bi, S., Koné, I., Wiafe, E. D., Osei, D., Wallis, J., Zinner, D.,…Galat-Luong,

A. (in press). Chlorocebus sabaeus - (Linnaeus, 1766). IUCN Red List of

Threatened Species.

Groves, C. P. (2001). Primate taxonomy. American Journal of Physical Anthropology,

118, 407–408.

Groves, C. P. (2005). Order primates. In D. Wilson & D. Reeder (Eds.), Mammal species

of the world: A taxonomic and geographic reference (3rd ed.) (pp. 111–184).

Baltimore, MD: The Johns Hopkins University Press.

91 Grubb, P., Butynski, T. M., Oates, J. F., Bearder, S. K., Disotell, T. R., Groves, C. P., &

Struhsaker, T. T. (2003). Assessment of the diversity of African primates.

International Journal of Primatology, 24(6), 1301–1357.

https://doi.org/10.1023/B:IJOP.0000005994.86792.b9

Guy, A. J. (2013). Release of rehabilitated Chlorocebus aethiops to Isishlengeni Game

Farm in KwaZulu-Natal, South Africa. Journal for Nature Conservation, 21(4),

214–216. http://doi.org/10.1016/j.jnc.2013.01.002

Guy, A. J., & Curnoe, D. (2013). Guidelines for the rehabilitation and release of vervet

monkeys. Primate Conservation, 27, 55–63. https://doi.org/10.1896/052.027.0103

Guy, A. J., Stone, O. M. L., & Curnoe, D. (2012). Assessment of the release of

rehabilitated vervet monkeys into the Ntendeka Wilderness Area, KwaZulu-Natal,

South Africa: A case study. Primates, 53(2), 171–179.

https://doi.org/10.1007/s10329-011-0292-0

Hall, K. R. L., & Gartlan, J. S. (1965). Ecology and behaviour of the vervet monkey,

Cercopithecus aethiops, Lolui Island, Lake Victoria. Proceedings of the

Zoological Society of London, 145, 37–57.

Harakas, M. (1995, July 25). Monkey mystery. Sun Sentinel. Retrieved from

https://www.sun-sentinel.com

Harrison, M. J. S. (1983). Patterns of range use by the green monkey, Cercopithecus

sabaeus, at Mt. Assirik, Senegal. Folia Primatologica, 41(3-4), 157–179.

doi:10.1159/000156129

Haus, T., Akom, E., Agwanda, B., Hofreiter, M., Roos, C., & Zinner, D. (2013).

Mitochondrial diversity and distribution of African green monkeys (Chlorocebus

9 2 gray, 1870). American Journal of Primatology, 75(4), 350–60.

http://doi.org/10.1002/ajp.22113

Healy, A., & Nijman, V. (2014). Pets and pests: Vervet monkey intake at a specialist

South African rehabilitation centre. Animal Welfare, 23, 353–360.

Henzi, S. P., & Lucas, J. W. (1980). Observations on the inter-troop movement of adult

vervet monkeys (Cercopithecus aethiops). Folia Primatologica, 33(3), 220–235.

doi:10.1159/000155936

Hill, C. M. (2000). Conflict of interest between people and baboons: Crop raiding in

Uganda. International Journal of Primatology, 21(2), 299–315.

https://doi.org/10.1023/A:1005481605637

Hill, C. M. (2004). Farmers’ perspectives of conflict at the wildlife-agriculture boundary:

Some lessons learned from African subsistence farmers. Human Dimensions of

Wildlife: An International Journal, 9(4), 279–286.

https://doi.org/10.1080/10871200490505710

Hill, C. M., & Webber, A. D. (2010). Perceptions of nonhuman primates in human-

wildlife conflict scenarios. American Journal of Primatology, 72(10), 919–924.

http://doi.org/10.1002/ajp.20845

Horrocks, J. A. (1986). Life-history characteristics of a wild population of vervets

(Cercopithecus aethiops sabaeus) in Barbados, West Indies. International Journal

of Primatology, 7(1), 31–47. https://doi.org/10.1007/BF02692308

Horrocks, J. A., & Baulu, J. (1988). Effects of trapping on the vervet (Cercopithecus

aethiops sabaeus) population in Barbados. American Journal of Primatology,

15(3), 223–233. https://doi.org/10.1002/ajp.1350150305

93 Horwith, B., & Lindsay, K. (1999, November). A biodiversity profile of St. Kitts and

Nevis. St. John’s, Antigua: Eastern Caribbean Biodiversity Programme, Island

Resources Foundation. Retrieved from

http://www.globalislands.net/userfiles/nevis_2.pdf

Huelsenbeck, J. P., & Ronquist, F. (2005). Bayesian analysis of molecular evolution

using MrBayes. In K. Dietz, M. Gail, K. Krickeberg, A. Tsiatis, & J. Samet

(Eds.), Statistical methods in molecular evolution (pp. 183–232). New York, NY:

Springer.

Hyler, W. (1995). Vervet monkeys in the mangrove ecosystems of southeastern Florida:

Preliminary census and ecological data. Florida Scientist, 58(1), 38–43.

https://www.jstor.org/stable/24320637

International Union for Conservation of Nature and Natural Resources (IUCN). (2019).

IUCN red list of threatened species. Retrieved from www.iucnredlist.org

Isbell, L. A. (1990). Sudden short-term increase in mortality of vervet monkeys

(Cercopithecus aethiops) due to leopard predation in Amboseli National Park,

Kenya. American Journal of Primatology, 21(1), 41–52.

https://doi.org/10.1002/ajp.1350210105

Isbell, L. A, & Pruetz, J. D. (1998). Differences between vervets (Cercopithecus

aethiops) and patas monkeys (Erythrocebus patas) in agonistic interactions

between adult females. International Journal of Primatology, 19(5), 837–855.

http://doi.org/10.1023/A:1020393329574

Isbell, L. A., Young, T. P., Jaffe, K. E., Carlson, A. A., & Chancellor, R. L. (2009).

Demography and life histories of sympatric patas monkeys, Erythrocebus patas,

94 and vervets, Cercopithecus aethiops, in Laikipia, Kenya. International Journal of

Primatology, 30(1), 103–124. https://doi.org/10.1007/s10764-009-9332-7

Jasinska, A. J., Schmitt, C. A., Service, S. K., Cantor, R. M., Dewar, K., Jentsch, J.

D.,…Freimer, N. B. (2013). Systems biology of the vervet monkey. ILAR

Journal, 54(2), 122–143. https://doi.org/10.1093/ilar/ilt049

Jones-Engel, L., Engel, G., Schillaci, M. A., Babo, R., & Froehlich, J. (2001). Detection

of antibodies to selected human pathogens among wild and pet macaques

(Macaca tonkeana) in Sulawesi, Indonesia. American Journal of Primatology,

54(3), 171–178. doi: 10.1002/ajp.1021

Kansky, R., Kidd, M., & Knight, A. T. (2016). A wildlife tolerance model and case study

for understanding human wildlife conflicts. Biological Conservation, 201, 137–

145. http://doi.org/10.1016/j.biocon.2016.07.002

Kavanagh, M. (1980). Invasion of the forest by an African Savannah monkey:

Behavioural adaptations. Behaviour, 73(3-4).

https://doi.org/10.1163/156853980X00258

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock,

S.,…Drummond, A. (2012). Geneious basic: An integrated and extendable

desktop software platform for the organization and analysis of sequence data.

Bioinformatics, 28(12), 1647–1649.

Kemper, M. (1979). History of Dania. Broward Legacy, 3(3-4), 10–15.

Kingdon, J. (1971). East African mammals: An atlas of evolution in Africa. New York,

NY: Academic Press.

95 Kingdon, J. (2015). The Kingdon field guide to African mammals. Princeton, NJ:

Princeton University Press.

Kingdon, J., & Gippoliti, S. (2008). Chlorocebus sabaeus. Retrieved from http:

https://www.iucnredlist.org/species/136265/4267012

Krige, P. D., & Lucas, J. W. (1975). Behavioural development of the vervet monkey in a

free ranging troop. Journal of Behavioural Science, 2(3), 151–160.

Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular Evolutionary Genetics

Analysis version 7.0 for bigger datasets. Molecular Biology and Evolution, 33(7),

1870–1874.

Kurita, H., Sugiyama, Y., Ohsawa, H., Hamada, Y., & Watanabe, T. (2008). Changes in

demographic parameters of Macaca fuscata at Takasakiyama in relation to

decrease of provisioned foods. International Journal of Primatology, 29(5),

1189–1202. https://doi.org/10.1007/s10764-008-9296-z

Lacy, R. C., & Pollack, J. P. (2014). Vortex: A stochastic simulation of the extinction

process [Computer software]. Brookfield, IL: Chicago Zoological Society.

Retrieved from http://www.vortex10.org/Vortex10.aspx

Lal, D., & Rajpurohit, L. S. (2010). Aggressiveness and the intensity of provisioning

(artificial feeding) hanuman langurs around jodhpur (Rajasthan). The Bioscan,

5(2), 259–262. Retrieved from

http://thebioscan.in/Journals_PDF/5219%20DEVI%20LAL.pdf

Lanfear, R., Frandsen, P. B., Wright, A. M., Senfeld, T., & Calcott, B. (2016).

PartitionFinder 2: New methods for selecting partitioned models of evolution for

96 molecular and morphological phylogenetic analyses. Molecular Biology and

Evolution, 34(3), 772–773. dx.doi.org/10.1093/molbev/msw260

Layne, J. (1997). Nonindigenous mammals. In D. Simberloff, D. C. Schmitz, & T. C.

Brown (Eds.), Strangers in paradise: Impact and management of nonindigenous

species in Florida (pp. 157–186). Washington, DC: Island Press.

Lee, P. C. (1984). Early infant development and maternal care in free-ranging vervet

monkeys. Primates, 25(1), 36–47. https://doi.org/10.1007/BF02382294

Lee, P. C. (2010). Sharing space: Can ethnoprimatology contribute to the survival of

nonhuman primates in human-dominated globalized landscapes? American

Journal of Primatology, 72(10), 925–31. http://doi.org/10.1002/ajp.20789

Lee, P. C., & Priston, N. E. C. (2005). Human attitudes to primates: Perceptions of pests,

conflict and consequences for primate conservation. In J. D. Paterson & J. Wallis

(Eds.), Commensalism and conflict: The human-primate interface (4th ed.) (pp.

1–23). Cambridge, UK: The American Society of Primatologists.

Legesse, M., & Erko, B. (2004). Zoonotic intestinal parasites in Papio anubis (baboon)

and Cercopithecus aethiops (Vervet) from four localities in Ethiopia. Acta

Tropica, 90(3), 231–236. https://doi.org/10.1016/j.actatropica.2003.12.003

Lernould, J. M. (1988). Classification and geographical distribution of guenons: A

review. In A. Gautier Hion, F. Bourliere, J.-P. Gautier, & J. Kingdon (Eds.), A

primate radiation: Evolutionary biology of the African guenons (pp. 54–78). New

York, NY: Cambridge University Press.

Lockwood, J. L., Hoopes, M. F., & Marchetti, M. P. (2013). Invasion ecology (2nd ed.).

Hoboken, NJ: Wiley-Blackwell.

97 Lowry, R. (2019). VassarStats: Website for statistical computation. Retrieved from

http://www.vassarstats.net

Lucas, M. L. (2014). Increasing certainty in an uncertain world: The importance of

signals and cues among male vervet monkeys (Master’s thesis). University of

Lethbridge, Alberta, Canada.

Madden, F. (2004). Creating coexistence between humans and wildlife: Global

perspectives on local efforts to address human-wildlife conflict. Human

Dimensions of Wildlife: An International Journal, 9(4), 247–257.

http://doi.org/10.1080/10871200490505675

Manfredo, M. J., & Dayer, A. A. (2004). Concepts for exploring the social aspects of

human-wildlife conflict in a global context. Human Dimensions of Wildlife, 4(9),

317–328. http://doi.org/10.1080/10871200490505765

McGuire, M. T. (1974). Historical, ecological, and population details. In H. Kuhn, W. P.

Luckett, C. R. Noback, A. H. Schultz, D. Starck, F. S. Szalay, & M. T. McGuire

(Eds.), The St. Kitts vervet (pp. 5–28). Los Angeles, CA: S. Karger.

McKinney, T. (2011). The effects of provisioning and crop-raiding on the diet and

foraging activities of human-commensal white-faced capuchins (Cebus

capucinus). American Journal of Primatology, 73(5), 439–48.

http://doi.org/10.1002/ajp.20919

Mekonnen, A., Rueness, E., Stenseth, N. C., Fashing, P. J., Bekele, A., Hernandez-

Aguilar, R. A.,…Roos, C. (2018). Population genetic structure and evolutionary

history of Bale monkeys (Chlorocebus djamdjamensis) in the southern Ethiopian

98 Highlands. BMC Evolutionary Biology, 18(1), 106.

https://doi.org/10.1186/s12862-018-1217-y

Meier, R., Shiyang, K., Vaidya, G., & Ng, P. K. L. (2006). DNA barcoding and

taxonomy in Diptera: A tale of high intraspecific variability and low identification

success. Systematic Biology, 55(5), 715–728.

https://doi.org/10.1080/10635150600969864

Messenger, A. M., Barnes, A. N., & Gray, G. C. (2014). Reverse zoonotic disease

transmission (Zooanthroponosis): A systematic review of seldom-documented

human biological threats to animals. PLoS ONE, 9(2), 1–10.

http://doi.org/10.1371/journal.pone.0089055

Miller, M. A., Pfeiffer, W., & Schwartz, T. (2010, November). Creating the CIPRES

Science Gateway for inference of large phylogenetic trees. In Proceedings of the

Gateway Computing Environments Workshop (GCE) (pp. 1–8). New Orleans,

LA: CIPRES Science Gateway.

Minnich, D. (Producer & Director). (1994). The Dania monkey story [DVD]. United

States: Wild World Video Productions.

Montayne, C. (1946, September 25). Monty says. The Miami News, Fort Lauderdale-

Hollywood, p. 2.

Mormile, J. E., & Hill, C. M. (2017). Living with urban baboons: Exploring attitudes and

their implications for local baboon conservation and management in Knysna,

South Africa. Human Dimensions of Wildlife: An International Journal, 22(2),

99–109. http://doi.org/10.1080/10871209.2016.1255919

99 Nekaris, A.-I., K., Boulton, A., & Nijman, V. (2013). An ethnoprimatological approach

to assessing levels of tolerance between human and commensal non-human

primates in Sri Lanka. Journal of Anthropological Sciences, 91, 219–231.

Nowak, K. (2013). Mangrove and peat swamp forests: Refuge habitats for primates and

felids. Folia Primatologica, 83(3–6), 361–376. http://doi.org/10.1159/000339810

Orams, M. B. (2002). Feeding wildlife as a tourism attraction: A review of issues and

impacts. Tourism Management, 23(3), 281–293. http://doi.org/10.1016/S0261-

5177(01)00080-2

Padial, J., Miralles, A., De la Riva, I., & Vences, M. (2010). The integrative future of

taxonomy. Frontiers in Zoology, 7(16). Retrieved from

https://doi.org/10.1186/1742-9994-7-16

Pasternak, G., Brown, L. R., Kienzle, S., Fuller, A., Barrett, L., & Henzi, S. P. (2013).

Population ecology of vervet monkeys in a high latitude, semi-arid riparian

woodland. Koedoe: African Protected Area Conservation and Science, 55(1).

https://doi.org/10.4102/koedoe.v55i1.1078

Patterson, L., Kalle, R., & Downs, C. (2017). A citizen science survey: Perceptions and

attitudes of urban residents towards vervet monkeys. Urban Ecosystems, 20(3),

617–628. https://doi.org/10.1007/s11252-016-0619-0

Patterson, L., Kalle, R., & Downs, C. (2018). Factors affecting presence of vervet

monkey troops in a suburban matrix in KwaZulu-Natal, South Africa. Landscape

and Urban Planning, 169, 220–228.

https://doi.org/10.1016/j.landurbplan.2017.09.016

100 Pimentel, D., Zuniga, R., & Morrison, D. (2005). Update on the environmental and

economic costs associated with alien-invasive species in the United States.

Ecological Economics, 52(3), 273–288.

http://doi.org/10.1016/j.ecolecon.2004.10.002

Stevens, C., & Powell, L. (2015, September 8). Wild monkeys thriving in Fort

Lauderdale topic of primate research. WSVN Channel 7 Miami/Fort Lauderdale.

Retrieved from https://wsvn.com/news/monkey-business/

Pruetz, J. D., & Isbell, L. a. (2000). Correlations of food distribution and patch size with

agonistic interactions in female vervets (Chlorocebus aethiops) and patas

monkeys (Erythrocebus patas) living in simple habitats. Behavioral Ecology and

Sociobiology, 49(1), 38–47. http://doi.org/10.1007/s002650000272

Rambaut, A. (2016). FigTree 1.4.3 [Computer software]. Retrieved from

http://tree.bio.ed.ac.uk/software/figtree/

Richardson, K. S. (1990). Space use by vervet monkeys (Cercopithecus aethiops) and its

consequences for the genetic structure of the Barbados population (Master’s

thesis). McGill University, Montreal, Canada.

Riley, E. P., & Wade, T. W. (2016). Adapting to Florida’s riverine woodlands: The

population status and feeding ecology of the Silver River rhesus macaques and

their interface with humans. Primates 57(2), 195–210.

https://doi.org/10.1007/s10329-016-0517-3

Roos, C., Zinner, D., Kubatko, L. S., Schwarz, C., Yang, M., Meyer, D.,…Osterholz, M.

(2011). Nuclear versus mitochondrial DNA: Evidence for hybridization in

101 colobine monkeys. BMC Evolutionary Biology, 11(77).

https://doi.org/10.1186/1471-2148-11-77

Saj, T. (1998). The ecology and behavior of vervet monkeys in a human-modified

environment (Master’s thesis). University of Calgary, Alberta, Canada.

Saj, T., Sicotte, P., & Paterson, J. D. (1999). Influence of human food consumption on

the time budget of vervets. International Journal of Primatology, 20(6), 977–994.

https://doi.org/10.1023/A:1020886820759

Schino, G., & Marini, C. (2014). Redirected aggression in mandrills: Is it punishment?

Behaviour, 151(6), 841–859. http://doi.org/10.1163/1568539X-00003174

Schorer, E. (1948, September 12). The jungle is her rival. The Philadelphia Inquirer, p.

22.

Self, S., Sheeran, L. K., Matheson, M. D., Li, J. H., Pelton, O., Harding, S., & Wagner, R.

S. (2013). Tourism and infant-directed aggression in Tibetan macaques (Macaca

thibetana) at Mt. Huangshan, China. Anthrozoos, 26(3), 435–444.

http://doi.org/10.2752/175303713X13697429463790

Sengupta, A., McConkey, K. R., & Radhakrishna, S. (2015). Primates, provisioning and

plants: Impacts of human cultural behaviours on primateecological functions.

PLoS ONE, 10(11), 1–14. https://doi.org/10.1371/journal.pone.0140961

Sengupta, A., & Radhakrishna, S. (2018). The hand that feeds the monkey: Mutual

influence of humans and rhesus macaques (Macaca mulatta) in the context of

provisioning. International Journal of Primatology, 39(5), 817–830.

https://doi.org/10.1007/s10764-018-0014-1

102 Sha, J. C. M., Gumert, M. D., Lee, B. P. Y. H., Fuentes, A., Rajathurai, S., Chan, S., &

Jones-Engel, L. (2009). Status of the long-tailed macaque Macaca fascicularis in

Singapore and implications for management. Biodiversity and Conservation,

18(11), 2909–2926. https://doi.org/10.1007/s10531-009-9616-4

Simberloff, D. (2003). How much information on population biology is needed to

manage introduced species? Conservation Biology, 17(1), 83–92.

http://doi.org/10.1046/j.1523-1739.2003.02028.x

Simberloff, D., Parker, I. M., & Windle, P. N. (2005). Introduced species policy,

management, and future research needs. Frontiers in Ecology and the

Environment, 3(1), 12–20. http://doi.org/10.1890/1540-

9295(2005)003[0012:ISPMAF]2.0.CO;2

Smith, J. H., King, T., Campbell, C., Cheyne, S. M., & Nijman, V. (2018). Modelling

population viability of three independent Javan gibbon (Hylobates moloch)

populations on Java, Indonesia. Folia Primatologica, 88(6), 507–522.

https://doi.org/10.1159/000484559

Stark, D., Nijman, V., Lhota, S., Robins, J., & Goossens, B. (2012). Modeling population

viability of local proboscis monkey Nasalis larvatus populations: Conservation

implications. Endangered Species Research, 16(1), 31–43.

https://doi.org/10.3354/esr00385

Struhsaker, T. T. (1967a). Behavior of vervet monkeys and other cercopithecines: New

data show structural uniformities in the gestures of semiarboreal and terrestrial

cercopithecines. Science, 156(3779),1197–1203.

103 Struhsaker, T. T. (1967b). Social structure among vervet monkeys (Cercopithecus

aethiops). Behaviour, 29(2-4), 83–121.

http://dx.doi.org/10.1163/156853967X00073

Struhsaker, T. T. (1971). Social behaviour of mother and infant vervet monkeys

(Cercopithecus aethiops). Animal Behaviour, 19(2), 233–250.

http://dx.doi.org/10.1016/S0003-3472(71)80004-0

Sugiyama, Y. (2015). Influence of provisioning on primate behavior and primate studies.

Mammalia, 79(3), 255–265. https://doi.org/10.1515/mammalia-2014-0028

Svardal, H., Jasinska, A., Schmitt, C. A., Huang, Y., Weinstock, G., Grobler,

P.,…Turner, T. R. (2017). Population genomics disentangles taxonomic

relationships and identifies ancient hybridization in the genus Chlorocebus

[Abstract]. American Journal of Physical Anthropology, 162(s64), 89.

Swofford, D. L. (2011). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other

Methods) (Ver. 4.0b10) [Computer software]. Sunderland, MA: Sinauer

Associates.

Takahashi, A. (2012). Male-male social interactions in vervet monkey: Targets and

tactics (Master’s thesis). University of Lethbridge, Alberta, Canada.

Turner, T. R., Cramer, J. D., Nisbett, A., & Patrick Gray, J. (2016). A comparison of

adult body size between captive and wild vervet monkeys (Chlorocebus aethiops

sabaeus) on the island of St. Kitts. Primates, 57(2), 1–10.

https://doi.org/10.1007/s10329-015-0509-8

104 Unwin, T., & Smith, A. (2010). Behavioral differences between provisioned and non-

provisioined barbary macaques (Macaca sylvanus). Anthrozoos, 23(2), 109–118.

https://doi.org/10.2752/175303710X12682332909855

U.S. Climate Data. (2019). Historical monthly average rainfall for Jan. 2014-Jan. 2018.

Retrieved from www.usclimatedata.com

U.S. Congress, Office of Technology Assessment. (1993, September). Harmful Non-

Indigenous Species in the United States (OTA-F-565). Washington, DC: U.S.

Government Printing Office. Retrieved from

https://www.anstaskforce.gov/Documents/OTA_Report_1993.pdf

Verbrugge, L. N. H., Van den Born, R. J. G., & Lenders, H. J. R. (2013). Exploring

public perception of non-native species from a visions of nature perspective.

Environmental Management, 52(6), 1562–1573. https://doi.org/10.1007/s00267-

013-0170-1

Wallis, J., & Lee, D. R. (1999). Primate conservation: The prevention of disease

transmission. International Journal of Primatology, 20(6), 803–826.

https://doi.org/10.1023/A:1020879700286

Westley, B. (1950). Chimp on my shoulder. New York City, New York E.P. Dutton.

Wheeler, R. J. (1990). Behavioral characteristics of the squirrel monkeys at the Bartlett

Estate, Ft. Lauderdale. Florida Scientist, 53(4), 312–316.

https://www.jstor.org/stable/24320403

Whitten, P. L., & Smith, E. O. (1984). Patterns of wounding in stumptail macaques

(macaca arctoides). Primates, 25(3), 326–336.

http://doi.org/10.1007/BF02382271

105 Wisely, S. M., Sayler, K. A., Anderson, C. J., Boyce, C. L., Klegarth, A. R., & Johnson,

S. A. (2018). Macacine herpesvirus 1 antibody prevalence and DNA shedding

among invasive rhesus macaques, Silver Springs State Park, Florida, USA.

Emerging Infectious Diseases, 24(2), 345–351.

https://doi.org/10.3201/eid2402.171439

Wolfe, L. D. (2002). Rhesus macaques: A comparative study of two sites Jaipur, India

and Silver Springs, Florida. In A. Fuentes & L. D. Wolfe (Eds.), Primates face to

face: The conservation implications of human-nonhuman primate

interconnections (pp. 310–330). Cambridge, United Kingdom: Cambridge

University Press.

Wolfe, L. D., & Peters, E. H. (1987). History of the free-ranging rhesus monkeys

(Macaca mulatta) of Silver Springs, Florida: 1938-1986. Florida Scientist, 50(4),

234–244. https://www.jstor.org/stable/24320179

Wolfe, N. D., Switzer, W. M., Carr, J. K., Bhullar, V. B., Shanmugan, V., Tamoufe, U.,

Tassy Prosser, A.,…Heneine, W. (2004). Naturally acquired simian retrovirus

infections in central African hunters. The Lancet, 363(9413), 932–937.

https://doi.org/10.1016/S0140-6736(04)15787-5

Wolfheim, J. H. (1983). Primates of the world: Distribution, abundance, and

conservation. Seattle, WA: University of Washington Press.

Wright, T. F., Eberhard, J. R., Hobson, E. A., Avery, M. L., & Russello, M. A. (2010).

Behavioral flexibility and species invasions: The adaptive flexibility hypothesis.

Ethology Ecology and Evolution, 22(4), 393–404.

http://doi.org/10.1080/03949370.2010.505580

106 Zulkifli, I. (2013). Review of human-animal interactions and their impact on animal

productivity and welfare. Journal of Animal Science and Biotechnology, 4(25), 1–

7. http://doi.org/10.1186/2049-1891-4-25

Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large

biological sequence datasets under the maximum likelihood criterion (Doctoral

dissertation). The University of Texas at Austin.

107