Interannual variation in the diets of Piliocolobus badius badius from the Taï Forest of Cote d’Ivoire

THESIS

Presented in Partial Fulfillment of the Requirements for the Degree Master of Arts in the Graduate School of The Ohio State University

By

Mary Alexandra Wilkins Graduate Program in Anthropology

The Ohio State University 2017

Master's Examination Committee:

W. Scott McGraw, Advisor Kristen Gremillion Mark Hubbe

Copyrighted by Mary Alexandra Wilkins 2017

Abstract

Resource specialists have low dietary diversity and a high reliance on certain food sources due to behavioral or morphological adaptations. Specialists, who rely on a narrow range of habitats or food sources, tend to have restricted geographic ranges and are vulnerable when their preferred foods diminish. Identifying the relative vulnerability of resident primate species is of vital importance as anthropogenic disturbances and large-scale climate change alter the availability of potential food sources. Long term data indicate that several species of East

African red colobus (Piliocolobus tephrosceles, Piliocolobus rufomitratus, and Piliocolobus kirkii) display significant inter and intra annual dietary variation. Much less is known about the extent of variation in the diets of West African red colobus. This study examines long term feeding data from one groups of Western red colobus (Piliocolobus badius badius) ranging in

Côte d’Ivoire’s Taï Forest to test the hypothesis that changes in phenological productivity have resulted in significant changes in dietary diversity. All data were collected by Amanda Korstjens

(2001) and assistants of the Taï Monkey Project. Feeding profiles were created through hourly scan samples, which indicate whether an individual was feeding and if so, what species and plant part was consumed. Phenological data were collected from 59 tree species on three transects biweekly; each tree was given an abundance score of 0 - 3. Shannon-Weiner Indices indicate significant decreases in dietary diversity between 1997 and 2015 (p<0.01). It is clear that fewer plant species are comprising a greater bulk of the diet over the study period. However, no apparent changes in phenological patterns of any individual plant parts were revealed. Further

ii analysis of nutritional components and other elements of selectivity is needed to identify why specific plants are so vital to the diets of P. badius badius. Identifying those elements of the red colobus diet that are vital, especially given the influence of climate change on forest production, is necessary for safeguarding all red colobus populations across Africa.

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Acknowledgments

I would like to thank my advisor, Dr. Scott McGraw, and my committee members, Dr. Mark

Hubbe and Dr. Kristen Gremillion for their support throughout this project. Additionally, this thesis - and many other projects - would not have been possible without the expertise, patience, guidance, and encouragement from the field assistants at the Taï Monkey Project. I extend an enormous merci to Benjamin, Frederic, Bertin, Richard, and many other friends at TMP.

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Vita

2011...... C.E. Jordan High School 2015...... B.A. Anthropology, History, Wake Forest University 2015 to present ...... Graduate Teaching Associate, Department of Anthropology, The Ohio State University

Publications Larsen PA, CH Hayes, MA Wilkins, Y Gommard, R Sookhareea, AND Yoder, SM Goodman. 2014. Population Genetics of the Mauritian Flying Fox, Pteropus niger. Acta Chiropterologica 16: 293-300.

Fields of Study

Major Field: Anthropology

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Table of Contents

Abstract ...... ii

Acknowledgments ...... iv

Vita ...... v

List of Tables ...... viii

List of Figures ...... x

Chapter 1: Introduction ...... 1

Specialists vs. Generalists: Definitions, Causes, and Vulnerabilities ...... 1

Red colobus as specialists ...... 5

Changes in the Taï Forest ...... 7

Habitat influences on red colobus ...... 8

Focus of Study and Implications ...... 9

Chapter 2: Materials and Methods ...... 11

Study Site ...... 11

Species Studied ...... 12

Data Collection ...... 13

Feeding Data Collection: ...... 13

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Phenological Data Collection: ...... 14

Analysis: ...... 15

Diet of P. badius badius ...... 15

Phenological Data: ...... 16

Chapter 3: Results ...... 18

Diet of P. badius badius ...... 18

Phenological Patterns ...... 20

Chapter 4: Discussion ...... 22

Chapter 5: Conclusions ...... 26

Changing Diets & Selectivity ...... 26

Specialization of P. badius badius...... 27

Conservation Implications ...... 28

References ...... 31

Appendix A: Figures ...... 39

Appendix B: Tables ...... 59

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List of Figures

Figure 1: A conceptual model of the niche breadths of specialists (S) and generalists (G) (Photo:

Devictor et al. 2010)...... 39

Figure 2: Predicted changes in niche breadths across different locations for specialists (a) and generalists (b) (Photo: Devictor et al. 2010)...... 40

Figure 3: Piliocolobus badius badius in the Taï Forest (Photo: Erin Kane) ...... 41

Figure 4: Côte d’Ivoire (Photo: Google Maps) ...... 42

Figure 5: A diagram of the TMP study grid and the home ranges of two groups of P. badius badius (Photo: Korstjens 2001)...... 43

Figure 6: Percent contribution to total diet when only the top ten most consumed species are considered in 1996, 1997 and 2015...... 44

Figure 7: The ripe fruit of Scytopetalum tieghemii ...... 45

Figure 8: Scytopetalum tieghemii mature leaves (Photo: Hawthorne and Jongkind 2006) ...... 46

Figure 9: Lophira alata mature leaves (Photo: Hawthorne and Jongkind 2006) ...... 47

Figure 10: Breakdown of total % contribution of each plant part to the diet in 2015. FU = unripe fruit, BU = unripe buds (closed flowers), LY = young leaves, FR = ripe fruit, LM = mature leaves...... 48

Figure 11: Comparison of Shannon-Weiner diversity indices for only common species between

1996 and 1997...... 49

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Figure 12: Comparison of Shannon-Weiner indices for only common species between 1997 and

2015...... 50

Figure 13: Comparison of Shannon-Weiner indices for the Top Ten species between 1996 and

1997...... 51

Figure 14: Comparison of Shannon-Weiner indices for the Top Ten species between 1997 and

2015...... 52

Figure 15: Interannual and seasonal variation in phenological scores of mature leaves...... 53

Figure 16: Interannual and seasonal variation in phenological scores of young leaves...... 54

Figure 17: Interannual and seasonal variation in phenological scores of unripe fruit...... 55

Figure 18: Interannual and seasonal variation in phenological scores of ripe fruit...... 56

Figure 19: Interannual and seasonal variation in phenological scores of open flowers...... 57

Figure 20: Interannual and seasonal variation in phenological scores of closed flowers...... 58

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List of Tables

Table 1: Plant species included in phenological transects...... 59

Table 2: All tree species consumed and percent contribution to diet in 1996, 1997, and 2015. .. 60

Table 3: The top ten most consumed plant species and their total percent contribution to dietary profiles for 1996, 1997, and 2015...... 64

Table 4: The percent contribution to diet of plant species consumed in all three sample periods.

...... 65

Table 5: Percent composition of the diet expressed as food items consumed during the 2015 sample period...... 66

Table 6: Shannon-Wiener indices of diversity (H) and Evenness scores (EH) for every year in three different comparisons...... 67

Table 7: Average monthly and annual phenology scores for mature leaves, young leaves, unripe fruit, ripe fruit, open flowers, closed flowers...... 68

Table 8: Mean annual phenological scores and Pearson’s Correlation Coefficient and p-Values for each plant part. LM = mature leaves, LY = young leaves, FR = ripe fruit, FU = unripe fruit,

FlC = closed flowers, and FlO = open flowers...... 69

Table 9: Mean annual phenological scores and Pearson’s Correlation Coefficient and p-Values for each plant part for Scytopetalum tiegemii. LM = mature leaves, LY = young leaves, FR = ripe fruit, FrU = unripe fruit, FlC = closed flowers, and FlO = open flowers...... 70

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Table 10: Mean annual phenological scores and Pearson’s Correlation Coefficient and p-Values for each plant part for Lophira alata. LM = mature leaves, LY = young leaves, FR = ripe fruit,

FU = unripe fruit, FlC = closed flowers, and FlO = open flowers...... 71

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Chapter 1: Introduction

Specialists vs. Generalists: Definitions, Causes, and Vulnerabilities

Any organism with a restricted niche breadth is said to be a specialist. An organism’s degree of specialization is the culmination of an evolutionary strategy of either 1) performing many activities fairly well, or 2) performing a few activities very effectively (Devictor et al. 2008, Ripley 1967). Specialists have behavioral or anatomical features that allow them to engage in a limited number of activities, but with extreme precision. For example, low quality foods that are difficult to process might select for anatomical features that aid consumption and digestion, such as complex gut systems or thick dental enamel (Daegling and McGraw 2007, McGraw et al. 2014, Lambert 2008).

Specializations may also come in the form of osteological features for locomotion through a particular habitat (McGraw 1998), variations in vocalization capabilities for long distance calling (Waser and Waser 1977), or unique optical features for nocturnality

(Barton 1998, Charles-Dominique 1977).

Animals can be specialized - or generalized - to a number of different ecological factors such as habitat type or food resources (Devictor et al. 2008, Hughes 2000,

Colwell and Futuyma 1971). Food resource specialists are those organisms which rely only on a select few resource types that constitute the bulk of the diet (Figure 1).

Generalists, on the other hand, rely on a wider variety of resources and have more heterogeneous diets than specialists. They may be able to consume a higher number of

1 tree species and/or more plant parts. It is not necessarily the raw number of different food sources consumed that distinguishes a resource specialist from a generalist, but the relative proportions (Emlen 1966, Newsome et al. 2009). For example, although a specialist primate may exploit a large number of food sources, when a small number of plant parts or tree species contribute to the bulk of the diet, they are considered a specialist. Yeager (1989) reported the proboscis monkey (Nasalis larvatus) consumed 55 plant species, but exhibited significant preference toward only two. The number and type of resources used over time in generalists can fluctuate more so than in specialists, who tend to experience dietary constancy over time (Kassen 2002).

Food resource specialists tend to have a competitive edge over generalists in exploiting specific resources due to some behavioral and/or morphological adaptations

(Marvier et al. 2004, Devictor et al. 2008). These specializations, such as long gut transit times related to large and complex gut systems, or sharp molar shearing crests allow them to process foods that are mechanically difficult or low in nutrition but can lead to reduced success in capturing or locating alternative food resources that may be outside the scope of their adaptations (Chapman et al. 2007, Lambert 1998, Ferry-Graham et al. 2002). For example, long gut transit times and narrow incisors may limit the total volume of food that can be processed in a given period of time (Lambert 1998, Lucas and Teaford 1994).

Primate species with long gut transit times must spend a greater proportion of the day feeding, and each feeding bout requires greater energy and time commitment (Milton

1981). Therefore, individuals with slow food passage rates must be more selective to ensure their foods will provide them with adequate nutrition.

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An organism’s specific vulnerability to extinction is determined by multiple factors, including large body size, ease of dispersal, low fecundity, and small geographic ranges (McGraw 2007, McKinney and Lockwood 1999). Another major factor contributing to an organism’s vulnerability may be dietary breadth. Specialists are particularly vulnerable under periods of rapid environmental change due to their dependence on certain types of food sources or habitat structures (Devictor and Robert

2009, Figure 2). If the abundance of their preferred food source decreases, they have limited options for fallback foods. Although specialists exhibit a competitive edge in processing particularly difficult foods over generalists, they tend to suffer when their preferred food source is eliminated through anthropogenic disturbance. Similarly, specialist animals have narrower geographic ranges than generalists, due to their dependence on particular foods or habitat structures (McKinney 1997).

A specialist’s decreased geographic range combined with their inability to process alternative foods, is commonly thought to place them under double jeopardy to local extirpation and extinction in the long term (Harcourt et al. 2002, McKinney 1997).

Therefore, specialists are more likely to be negatively affected by global changes than are generalists. As environments change and food resources become less diverse and less abundant due to fragmentation, degradation and foreign species invasions (Devictor et al.

2008), human induced changes tend to act as a non-random filter against specialist species. That is to say, ecological winners (generalists) and losers (specialists) are not randomly distributed (McKinney and Lockwood 1999). Indeed, studies have shown that

3 specialists tend to occur less in fragmented forests and rapidly changing environments, where their competitive edge has been rescinded (Devictor et al. 2008).

Folivorous primates have behavioral and morphological adaptations reflecting their evolutionary strategy as specialists (Struhsaker 2010). Although foliage in primary rainforests is distributed relatively evenly, many folivorous primates select only certain types of leaves (Chapman and Chapman 2002). Not only do folivorous primates engage in selective behaviors, but they also have morphological adaptations which allow them to consume tough, fibrous foods that are difficult to digest (Ferry-Graham et al. 2002).

Other key adaptations possessed by folivorous primate species are large multi-chambered stomachs and long gut transit times, wherein ingested vegetation can be retained and fermented by efficient resident microorganisms, providing better access to the nutritional qualities of the food (Mowry et al. 1996). While such adaptations provide folivorous primates with the ability to efficiently digest leaves, they hinder the primate’s ability to consume enough high-quality food, such as fruit, to meet their nutritional requirements

(Lambert 1998, Milton 1981). The fact that folivorous primates tend to be highly selective poses a paradox, considering that the literature traditionally identifies frugivorous primates as selective and vulnerable (Johns and Skorupa 1987). Although the specialized anatomy of the red colobus allows them to exploit foliage, which is far more abundant than fruit, red colobus still exhibit high levels of selectivity for certain types of foods. This present study addresses which plant species are most import in the diets of P. badius badius.

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Red colobus as specialists

Red colobus are cercopithecoid monkeys in the subfamily colobinae.

Approximately 16 species of red colobus make up the genus Piliocolobus, one of three

African colobine genera. Based on expansive studies at primarily three sites in East

Africa, we know that population densities of three red colobus species (P. tephrosceles,

P. kirkii, and P. rufomitratus) positively correlate with the presence of preferred tree species (Chapman and Chapman 1999, Mbora and Meikle 2004, Siex and Struhsaker

1999). Previous studies have shown that some red colobus exhibit dietary plasticity, but remain highly sensitive to habitat quality, and populations tend to decline on the periphery of pristine forests (Chapman and Chapman 1999, Chapman et al. 2007,

Struhsaker 2005) because they rely on high canopy cover for anti-predation strategies, and substrate preference. Far less research of this type has been conducted on West

African red colobus populations, including P. badius badius (Figure 3).

All red colobus species have morphological specializations for a diet consisting primarily of foliage including complex, ruminant guts and high-crested molars (Lucas and Teaford 1994, Struhsaker 2005). Colobines are the only primates that exhibit a digestive strategy of foregut fermentation, while other leaf-eating primates have an enlarged caecum and/or colon (Lambert 1998). Population densities have also been noted to correlate with the presence of particular tree species (Johns and Skorupa 1987), signaling that red colobus are generally considered to be highly specialized when compared to other primate species (Struhsaker 2010). Additionally, red colobus tend to

5 select younger leaves and unripe fruits, that are high in protein but low in acidity or fiber content (Chapman and Chapman 2002, Mowry et al. 1996, Struhsaker 2010).

Despite certain dietary restrictions and their classification as resource specialists, red colobus populations are known to alter the types and quantities of foods that are consumed in response to changes in forest structure (Chapman and Chapman 1999). For example, in the late 1980s, a population of Procolobus badius rufomitratus was observed to consume more mature leaves, which are lower in nutritional quality and higher in antifeedants. This was most likely a response to habitat changes due to intense logging of the Mchelelo Forest in Kenya in the 1960s and 1970s (Decker 1994, Mowry et al. 1996).

Changes in food availability therefore have strong effects on population size in colobus monkeys (Chapman et al. 2007), showing that dietary specializations pose certain problems not only for meeting nutritional requirements, but also for population sustainability and conservation.

P. badius in Kibale National Park have been noted to alter their day range and speed of travel rather than change their diet in response to food scarcity (Chapman and

Chapman 2002). Red colobus are also known to vary in group size and ranging behavior over space and time (Chapman et al. 2002), but fewer longitudinal studies have investigated how diet changes over time given changing environments. Potential responses to changes in food availability and habitat structure must be fully understood and dietary preferences must be analyzed in order to better inform conservation efforts.

Such efforts include identifying which tree species are particularly important in the primate’s diet.

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Many studies have presented information about red colobus in East Africa, but much less is known about variation in the diets of West African taxa, including

Piliocolobus badius badius. This species of red colobus appears to have a highly specialized diet (Chapman et al. 2002, Mowry et al. 1996), which can increase population vulnerability when faced with alterations in forest structure. In fact, P. badius badius is most abundant in undisturbed forests and especially sensitive to environmental changes

(Johns and Skorupa 1987, McGraw 2007, Struhsaker 2005).

Changes in the Taï Forest

Over the past twenty years, the Taï Forest in Côte d’Ivoire has experienced transformations, including changes in rainfall and fragmentation due to global climate change as well as local political instability and a subsequent inability to enforce logging regulations. Data show rainfall has declined from the early 1990s to the present

(Anderson et al. 2005, Polansky and Boesch 2013), a phenomenon which may lead to differential fruit production. In general, there is a positive correlation between fruiting production efforts of trees and water availability. High water availability may enhance germination success and subsequently the presence of fleshy fruit (Anderson et al. 2005).

Although there is some disagreement on the correlation between fruit production and rainfall (Polansky and Boesch 2013), it is clear that areas of West Africa, including the

Taï Forest are undergoing significant reductions in the amount of rainfall in the past decades.

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A second major driver of change in the Taï Forest is deforestation, which may lead to the reduction of tree species diversity. Such diversity is critical for the survival and maintenance of certain specialists, including red colobus. Political instability in Côte d’Ivoire has posed problems for policy regulation and enforcement of laws designed to protect the forest, leading to an overexploitation of lumber dating back to the 1960s

(Mowry et al. 1996). This fragmentation has compromised the forest’s ability to regenerate (Chatelain et al. 1996), which further threatens resident primate populations by reducing canopy pathways and increasing the energetic demands of finding food

(Chapman et al. 1997). Logging and forest fragmentation drastically decreases the amount of diversity in the affected area (Chapin et al. 2000), including the availability of potential food sources.

Habitat influences on red colobus

Environmental degradation is one of the greatest threats to red colobus across

Africa (McGraw 2007, Struhsaker 2005). Most of the remaining viable populations of red colobus occur in well-protected national parks such as the Taï Forest (Struhsaker 2010).

Healthy forest preserves are vital for the survival of all red colobus taxa, but even the largest remaining forests are undergoing drastic changes in structure, composition and size (Murphy and Lugo 1986, Chapman et al. 2007, Chapman et al. 2006, Chatelain et al.

1996, Chapin et al. 2010).

Dietary sensitivity of P. badius badius is potentially problematic given recent trends in the forest ecology of Côte d’Ivoire (Bitty et al. 2015, McGraw 2007). As

8 resource specialists, red colobus are likely to be negatively impacted by decreasing food resource diversity and forest fragmentation. Changes in food availability will require P. badius badius to respond in ways that do not compromise their nutritional intake, and are constrained by their anatomical structures. When there are changes in food availability, specialists such as the red colobus will need to adjust their foraging behavior more than resource generalists, or change their diet. If species presence and abundance patterns are indeed changing within the forest, P. badius badius will need to adjust their diet or exert energy to conserve their original diets.

Focus of Study and Implications

This project examines the relationship between diet and food abundance in a red colobus group (P. badius badius) in Côte d’Ivoire’s Taï Forest. The first goal of this project is to quantify the degree of specialization in a group of Taï P. badius badius. Red colobus in Uganda, Kenya and Zanzibar are known to change their diet in response to environmental stressors (Struhsaker 2010, Chapman and Chapman 1999, Mbora and

Meikle 2004). I apply this same question to a group of West African Red colobus determine the degree to which P. badius badius in Taï National Park have shown levels of increasing specialization. This paper addresses the following questions: is there directional interannual variation in the diets of P. badius badius over a twenty-year time period? Specifically, is dietary breadth decreasing? If dietary changes are indeed occurring in this group of P. badius badius, are they correlated with changes in forest structure?

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It has been suggested that environmental degradation is the primary threat to primate biodiversity (Olden 2006), and P. badius badius has been identified as the most vulnerable primate species in the Taï Forest due to their body size, habitat sensitivity, and response to humans (McGraw 2007). This paper ultimately contributes to the overall understanding of P. badius badius’ nutritional requirements by identifying which food sources have remained a significant portion of the diet despite changes in preferred food source over time.

Given P. badius badius’ presumed natural history as a food resource specialist

(Nowak and Lee 2013) and the rapidly changing forest structure of the Taï Forest

(Chatelain et al. 1996), a full understanding of the nutritional requirements of their dietary profiles is required to help safeguard this endangered species. Nearly all red colobus species are endangered and many face extinction in the near future (Chapman and Chapman 1999, Struhsaker 2005). Although there are ample data sets on dietary profiles of red colobus, much less is known about West African red colobus.

Additionally, because no red colobus have been successfully maintained in captivity, there is certainly room for identifying which food sources are most important for red colobus during times of ecological stress. The research presented here will further our knowledge of how one red colobus species is able to adjust to a changing environment.

By revealing how primates meet their nutritional requirements given changing environments, this study attempts to shed light on the ways that the diet of P. badius badius has exhibited increasing trends specialization due to changes in forest structure.

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Chapter 2: Materials and Methods

Study Site

This thesis utilizes data collected a nineteen-year period collected by Amanda

Korstjens, and the field assistants of the Taï Monkey Project (TMP). All data were collected in the Taï National Park in south-western Côte d’Ivoire (0˚15’ - 6˚07’N, 7˚25’

W - 7˚54’W) (Figure 4). All research was conducted in conjunction with the Taï Monkey

Project (TMP) in the TMP primary research grid. The Taï Forest is classified as a tropical evergreen seasonal lowland forest with distinct wet and dry seasons (Korstjens 2001,

Stoorvogel 1993). It receives an average rainfall of 1893 mm annually (Anderson et al.

2005). Temperatures in the Taï Forest range between 24 - 28 ℃ on average (Doran

1997). The Taï Forest is home to many mammals, including nine higher primate species:

Red colobus (Piliocolobus badius badius), olive colobus (Procolobus verus), black and white colobus (Colobus polykomos), Diana monkeys (Cercopithecus diana), Campbell's monkeys (Cercopithecus campbelli), Putty-nosed monkeys (Cercopithecus nictitans), lesser spot-nosed monkeys (Cercopithecus petaurista), sooty mangabeys (Cercocebus atys), and the common chimpanzee (Pan troglodytes) (McGraw 2007).

Taï Forest is the largest undisturbed portion of the Upper Guinea Forest and remains an important focus for conservation efforts (McGraw and Zuberbühler 2007).

However, the forest has been heavily fragmented in the past century. The Taï Forest and its resident primate species have been increasingly subjected to anthropogenic 11 disturbances such as deforestation, illegal poaching for bushmeat trade, and mining (Bitty et al. 2015, Chatelain et al. 1996, Lewis 2009, McGraw 2007). Political instability in recent decades has led to the inability of government agencies to enforce policies aimed at reducing these pressures (Struhsaker 2005). Many of Taï’s primates are classified as endangered or vulnerable, contributing to the urgency of conservation efforts targeted at the forest. In fact, Taï National Park is thought to be the last remaining habitat for healthy populations of P. badius badius (Struhsaker 2005).

Studies of the Taï Forest’s primates commenced in the 1970s, beginning with chimpanzees (Boesch 1978, Boesch and Boesch 1989). The Taï Monkey Project (TMP) was established by Ronald Noë and Bettie Sluijter in 1989 and hosted its first students in

1991. The research station for TMP is on the western border of the forest, 20 km from the nearest village (McGraw and Zuberbühler 2007). The home range of the red colobus group that was studied falls inside the TMP study grid (Figure 5).

Species Studied

Colobines are predominantly folivorous Cercopithecoid monkeys found across

Africa and Asia (Sterk 2012). African colobines are divided into three genera: Colobus

(black and white colobus), Procolobus (olive colobus), and Piliocolobus (red colobus) which diverged approximately 6-8 million years ago (Ting 2008). Piliocolobus can be found across the northern half of the continent, ranging from Tanzania and Zanzibar in the east, to Senegal and the Gambia in the west (Struhsaker 2010). The subspecies that is the focus of this project, Piliocolobus badius badius ranges from Sierra Leone to the

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Bandama River in Côte d’Ivoire. It is most abundant in the Taï Forest (McGraw and

Zuberbühler 2007).

P. badius badius are large-bodied monkeys with deep red and black pelages

(Figure 3). P. badius badius is a large bodied colobine, with a mean male body weight of

8.3kg, and mean female body weight of 8.2kg (McGraw and Zuberbühler 2007). At Taï, red colobus live in large groups of between 40 - 60 individuals, which regularly engage in fission fusion behavior, especially when resources are scarce (McGraw and Zuberbühler

2007). Many species of Piliocolobus, including badius are listed as endangered on the

IUCN red list (2016). The home range of the study group, which is colloquially known as

Badius 2 ranges from 500m EW by 800m NW within the TMP grid. P. badius badius are considered the most vulnerable primate species in the Taï Forest due to their reliance on pristine forest, large body and group sizes, response to human presence and substrate preference (McGraw 2007).

Data Collection

Feeding Data Collection

The data discussed in this thesis are derived from three sample periods over 19 years: 1996, 1997, and 2015. There are only seven months of the year that are available in all three years. Therefore, this thesis compares feeding data on red colobus collecting during January, February, March, April, May, October, and November of each year. Data from 1996 and 1997 were taken from Korstjens (2001) and samples from 2015 were collected by TMP local field assistants using the same methodology as Korstjens (2001).

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Feeding data in all sample periods were collected during hourly food scans of all individuals within sight of the observer. Hourly scans were collected between 07:00 -

17:00 hours. During data collection, each individual was identified by age and sex by local field assistants of the Taï Monkey Project. If any individuals were feeding, the plant species and plant part (young or mature leaves, ripe or unripe fruit, flowers, seeds, termites, or liana species) were noted to construct a feeding profile. The percent contribution of each plant species to the total diet was calculated for each species in all three time periods.

Phenological Data Collection

All phenological data were collected by local TMP field assistants biweekly from

2006 to 2014 on approximately 57 different species. Tree species included were found on three transects in the main study grid of the TMP research site. Transects run North-

South through the home ranges of the study group, and are 1000m x 25m. During data collection, the phenological state of each individual tree was visually assessed using a 0 -

3 percentage scale. Each individual tree was given a score from 0 (no presence) to 3

(fully abundant) for abundance of six different plant parts: mature leaves, young leaves, ripe fruit, unripe fruit, open flowers, and closed flowers. A full list of tree species identified can be found in Table 1. Many of the tree species on the transects are not consumed by P. badius badius, but all commonly consumed plant parts in 2015 are present in the transects, and the phenological data provides indices total availability for individual plant parts.

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Phenological data are not continuously available; therefore, I only consider three sample periods 2006, 2009, and 2014 for the months of January, February, March,

October, and November. As a result, the results do not give a full picture of seasonal variation in phenological patterns, and general conclusions are only limited to a few months from the year. Furthermore, phenological data are not available prior to 2005 and as a result, I am unable to compare dietary diversity of P. badius badius from 1996 or

1997 to total phenological abundance. The comparison, however, does allow for general conclusions about changes in forest productivity over time.

Analysis

Diet of P. badius badius

The total number of species consumed in each period was recorded, and the percent contribution to total diet was calculated for each species. Qualitative comparisons were used to assess the changes in individual plant species. The percent of total fruit content in the diet was also calculated to assess changes in total fruit consumption.

In order to adequately reflect all possible changes in diet occurring between the three sample periods (1996, 1997, and 2015), I calculated indices of specialization to reflect diversity of diets. Indices were compared in three different ways. First, I compared the three sample periods when all consumed plant species were considered. Second, I only considered plant species that were consumed during all three categories. These are referred to as common species. The third comparison for analysis only takes into consideration the top ten most consumed species for each sample period.

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In order to gauge the diversity of the diet, I used the Shannon-Wiener Index of diversity, a common index that reflects species diversity within a community. The

Shannon-Wiener index is typically used in community ecology surveys by analyzing raw counts of presents species. It may also be used for analyzing diversity of foods that are present in animal diets (Ng’endo et al. 2016). The Shannon-Wiener index (H) was calculated using the formula: H’ = - Σ pi ln pi . I also calculated the Evenness Scores of species present for the Shannon-Weiner index, which reflects relative contribution of each individual plant species to the diet. This score takes into consideration the equitability of species exhibited in the diets of P. badius badius. Evenness, or equitability, was calculated using the equation EH = H / lnS. Total evenness is reflected by a “1” while a complete disparity between all values is represented by a “0.” Both the

Shannon-Weiner index and evenness scores were calculated for all three conditions (all, common, and top ten) for 1996, 1997, and 2015.

In order to determine whether Shannon-Weiner indices were significantly different, I used the Hutcheson’s t-test, which has been used to assess differences in diversity of forest structures and animal communities (Hutcheson 1970, Jackson et al.

2016, Oliveira et al. 2007). The t value can be calculated using the formula: t = Ha - Hb

2 2 √ (S Ha + S Hb).

Phenological Data

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To assess changes in forest phenology over time, the total abundance of different plant parts within the TMP study grid were compared from each sample period (2006,

2009, 2014) for January, February, March, October, and November. I created weighted average abundances scores for each tree species and plant part per month. In order to account for seasonality, I pooled and averaged each monthly phenological score to create mean annual productivity scores for each plant part: mature leaves, young leaves, ripe fruit, unripe fruit, closed flowers, open flowers. Mean productivity scores are also broken down by plant species for the only two species that were consumed by P. badius badius across all three sample periods: Scytopetalum tieghemii and Lophira alata. Interannual variation in mean productivity scores can be assessed using Pearson’s correlation coefficient (Cleland et al. 2007, Chapman et al. 2005). Pearson’s correlation coefficient between year and average productivity score was calculated for each individual plant part, as well as for S. tieghemii and L. alata, using the formula:

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Chapter 3: Results

Diet of P. badius badius

During the seven months analyzed, P. badius badius consumed 84 unique species in 1996, 76 species in 1997, and 34 species in 2015 (Table 2) Raw counts of species consumption reveals that the total number of species consumed in the seven-month sample period decreased between 1996 and 2015.

Not only did the total number of species in the diet decrease, but fewer species comprise the bulk of the diet. When only the top ten species are considered, the total contribution to diet was 57.71% in 1996, 63.06% in 1997, and 86.26% in 2015 (Figure

6). The percent contribution of each plant species within the top ten most consumed species for each sample period is in Table 3. Two species were among the top ten most consumed plants during all three sampling periods: Scytopetalum tieghemii (Figures 7,8) and Lophira alata (Figure 9)

When only the common species are considered for each sample period, the species that increased in proportion were Anthonotha fragrans, Calpocalyx brevivracteatus, Irvingia gabonensis, Oldfelida africana, Pentaclethra macrophylla,

Piptadeniastrum africanum, and Scytopetalum tieghemii (Table 4). The data show that total diversity decreased from 1996 to 2015, the relative contribution of fewer plants increased.

18

The percent contribution of different plant parts is not available for all sample periods, and therefore cannot be analyzed over time. However, the total percent contribution of each plant part to the diet in 2015 can be found in Table 5 and Figure 10.

I examine specialization using two indices: The Shannon-Wiener Index, which reflects dietary diversity, and an Evenness Score which reflects relative contribution of each individual plant species to the diet. I present Shannon-Wiener Indices and Evenness

Scores for each sample period (1996, 1997, 2015) that derive from three separate considerations:

1) All plant species

2) Only plant species that are consumed in all sample periods (common

species)

3) The top ten most frequently consumed plants in each sample period

Shannon-Weiner Indices revealed that overall dietary diversity and evenness decreased between 1996 and 2015 regardless of which comparisons were made (all species, common species, top ten species) (Table 6).

When all plant species consumed in each period were considered the following

Shannon-Wiener and evenness scores were H=3.437 and EH = 0.778 in 1996; H=3.285 and EH = 0.781 in 1997, and H=2.195 and EH = 0.628 in 2015. A Hutcheson’s t-test of significance revealed that the changes between 1996-1997 were not significant (t=0.787, p= 0.432), but the reduction in diversity from 1997-2015 was significant (t= 4.9, p <

0.01).

19

For only common species that were consumed in all three periods, H=2.557, EH =

0.840 in 1996; H=2.433 and EH = 0.799 in 1997; and H=1.662 and EH = 0.546 in 2015.

The Hutcheson’s t-test revealed no significant difference between 1996 and 1997

(t=0.599, p=0.549) (Figure 11), but significant reductions in diversity from 1997 to 2015

(t = 3.503, p < 0.01) (Figure 12).

When only considering the top ten species consumed in each period, H = 2.089 and EH = 0.907 in 1996; H = 2.014 and EH = 0.874 in 1997; and H=1.805 and EH = 0.784 in 2015. The Hutcheson’s t-test revealed no significant difference between 1996 and

1997, (t=0.537, p=0.549) (Figure 13) and no significant difference between 1997 and

2015 (t=1.918, p=0.057). However, there was a significant difference between the diversity scores of 1996 and 2015 (t=2.520, p=0.013) (Figure 14).

Phenological Patterns

The average annual abundance scores for mature leaves, young leaves, unripe fruit, ripe fruit, open flowers, and closed flowers can be found in Table 7. Although there are slight detectable changes in the total availability of various plant parts interannual, no statistically significant long-term changes in phenological productivity were revealed by this study. Mature leaves were most consistently abundant (Figure 15), while young leaves were less available, especially during 2014 (Figure 16). Unripe fruit was more available than ripe fruit, but both exhibited similar degrees of annual change between

2006 and 2014 (Figure 17, Figure 18). Both open and closed flowers were least available in 2014, but no overall change was detected (Figure 19, Figure 20). Pearson’s

20

Correlation Coefficient was calculated to standardize mean phenological scores and determine the significance of any long-term changes. Despite minor fluctuations in mean annual phenological scores for various fruit parts, the Pearson’s Correlation revealed the mean annual phenological index did not vary as a function of year for any of the six different plant parts (Table 8).

Mean annual phenological scores were also calculated for plant parts (unripe fruit, ripe fruit, mature leaves, young leaves, open flowers, and closed flowers) of two trees:

Scytopetalum tieghemii and Lophira alata. For S. tieghemii, there were no changes in any plant parts except for open and closed flowers (Table 9). L. alata exhibited slightly more fluctuation in the total availability of leaves, fruit, and flowers. What is most apparent about the changes in availability of L. alata are the increases in fruit and flowers between

2006 and 2014 (Table 10).

21

Chapter 4: Discussion

Results from an analysis of P. badius badius diets at three points over a nineteen year time period reveal striking differences between the late 1990’s and 2015, both in overall diversity and equitability of species consumption. From these results, we can draw several conclusions about the ways diets of western red colobus in Taï National

Park changed. First, it is clear that overall dietary diversity has declined significantly. Not only did the total number of species consumed decrease from 100 to 34, but Shannon-

Weiner indices consistently declined from 1996 and 1997 to 2015. This was true regardless of whether one considers all plant species, common species, or only the top ten species for each time period.

Not only did overall dietary diversity, but equitability of species consumed was also reduced. Because raw counts of species presence / absence within the diet does not consider total abundance, I also calculated the evenness scores of all Shannon-Weiner indices. Results show that all evenness scores decreased from 1996 to 2015, indicating that P. badius badius became more reliant on fewer species than they have in the past.

These changes can also be seen upon further analysis of the top ten most consumed species for each year. For example, Scytopetalum tieghemii, Dialium aubrevillei and

Calpocalyx brevibracteatus contributed to 66% of the total diet in 2015, but only 20.11%

22 in 1996 and 30.87% in 1997. These data suggest P. badius badius are relying on a fewer number of species to make up a greater bulk of the diet.

Analysis of the top ten most consumed species in 1996, 1997 and 2015 reveals an additional trend in P. badius badius diets. Only two species ranked within the top ten most consumed species during all three periods: Scytopetalum tieghemii, which consistently ranked first by a wide margin, and Lophira alata. With regard to the latter, the total percent contribution of L. alata decreased over time from 8.62% in 1996 to

2.51% in 2015. The overlap of the top ten most consumed species in 1996 and 1997 was seven species: S. tieghemii, L. alata, Berlinia grandiflora, Diospyros-sanza minika,

Combretum aphanopetalum, Coula edulis, and Ricinodendron heudelotii. However, between 1997 and 2015, only four species were common to the top ten: S. tieghemii, L. alata, Dialium aubrevillei, and Gilbertiodendron preussii.

These data suggest that despite P. badius badius’ characterization as a particularly specialized animal, there appears to be a considerable turnover in the species that contribute to the majority of the diet during different time intervals. What is noteworthy, however, is that ripe fruit and young leaves of Scytopetalum tieghemii is consistently the most consumed species by a considerable margin. It is clear that P. badius badius exhibits a heavy reliance on this particular species. It is important to keep in mind that a specialized diet does not necessarily mean that animal eats only a limited number of species. Rather, it may exhibit a heavy reliance on a select few food sources (Ford et al.

1998), as is the case with P. badius badius.

23

Although red colobus are highly abundant in pristine, high-canopy forests, they invariably suffer in forest fragments (Chapman et al. 2002, Johns and Skorupa 1987,

Mowry et al. 1996, McGraw 2007, Struhsaker 2005). Red colobus living in fragments and/or undergoing food stress exhibit higher levels of parasitic infection (Chapman et al.

2006), reduced microbiota efficiency and richness, impeding their ability to digest fructose and mannose (Barelli et al. 2015), higher cortisol levels (Chapman et al. 2007), and increased day ranges (Chapman and Chapman 2002). Unlike other red colobus species, there are no populations of P. badius badius living in forest fragments, which reveals the importance of pristine forest to the maintenance of viable populations. The present study reveals significant changes in the diets of P. badius badius, but what remains to be investigated is whether or not they are suffering due to these dietary contractions.

There are several potential explanations for what might induce dietary changes, including fluctuations in dominant food source productivity. Phenological analyses revealed no significant correlations between sampling period and total phenological availability for any plant part. Poor correlations may be a reflection of inconsistent sampling methods and the fact that data are not continuous from 2006 to 2014. The phenological sample period in this study only included five months and three years from this time period. It is entirely possible that major changes in phenological patterns occur outside the parameters of this study and are therefore not captured. Although transects were created to be representative of the TMP study grid at large, perhaps such a limited sample is not reflective of potentially larger changes at the community level. It also may

24 be possible that an 8-year focus is simply not a large enough time period to capture long- term changes in forest structure (Clutton-Brock and Sheldon 2010, Rees et al. 2001).

Despite poor correlations between annual sample period and total abundance, we can still draw descriptive conclusions from the present phenological data. The most frequently consumed plant parts in 2015 were unripe fruit, young leaves, closed flowers, and unripe fruit. This is particularly interesting, given that unripe fruit, young leaves, and closed flowers consistently produced the lowest mean annual phenological scores. This may signify that P. badius badius are actively selecting plant parts that are not necessarily widely available. Furthermore, it is clear that the productivity of Lophira alata fruit, flowers, and leaves is actually increasing but is not reflected in P. badius badius feeding profiles. Lophira alata was present in the diets from all three sample periods (1996, 1997 and 2015) but it decreased in its total contribution to the diet from

1996 to 2015. It is intriguing that despite the increased presence of Lophira alata fruit, flowers, and young leaves the total percent contribution to diet decreases.

25

Chapter 5: Conclusions

Changing Diets & Selectivity

Similar to previous studies on red colobus in Uganda, Kenya, and Zanzibar

(Chapman and Chapman 2002, Chapman et al. 2006, Chapman et al. 2007, Mowry et al.

1996) a group of P. badius badius in Taï National Park exhibit dietary variation over time. Trends revealed in this study include an increased reliance on certain types of foods and decreasing total dietary diversity. The data suggest that over this sampling period, the diets of P. badius badius became more restricted and fewer plant species contributed to the bulk of the diet. Studies on primate diets have pointed to external factors including total plant availability or nutritional breakdown as predictive of selectivity (Chapman and

Chapman 1999, Rothman 2015). Phenological analysis from this study did not reveal significant changes in productivity of various plant parts; however we cannot rule out the possibility that P. badius badius diets are changing as a function of changing forest structures. Many studies have revealed the positive correlations between temperature, water availability, and various aspects of phenology including productivity and seasonal timing (Baddeck et al. 2004, Visser and Both 2005, Walther et al. 2002). The data presented here are extremely limited and must be expanded upon for a full understanding of phenological changes in the TMP study grid. It will be vital to continue collecting

26 phenological data in the Taï Forest in order to better monitor plant productivity as temperatures, rainfall, and pollution levels continue to change in the future.

A second explanation for why certain plant species are consumed at such high frequency may be related to their nutritional components. Multiple frameworks within nutritional ecology serve to explain dietary selectivity, including energy maximization or nutritional geometry (Felton et al. 2009 Rothman et al. 2011, Rothman 2015). Nutritional geometry is a framework that has been used to determine how primates balance their varying nutritional needs. It has been suggested that specific nutritional components of foods, such as protein or fiber, have the possibility to influence an individual's internal homeostasis as well as external performance (Raubenheimer et al. 2009, Raubenheimer and Simpson 2012). Past studies have shown that populations of East African red colobus tend to select foods that are high in protein and low in fiber (Chapman and Chapman

2002, Mowry et al. 1996). These same studies have shown that although consumption of plant species may exhibit geographic or temporal variability, the composition of macronutrients tends to remain more stable. A nutritional analysis of the phytochemical composition of plant parts consumed by P. badius badius in Taï may reveal the specific nutritional requirements needed to sustain viable populations. Recent studies of black and white colobus highlight the utility of this approach (Dunham, 2017).

Specialization of P. badius badius.

Red colobus are consistently defined as resource specialists due to their specific anatomical specializations (Chapman and Chapman 2002, Struhsaker 2010), and indeed,

27 results from this study suggest that P. badius badius increased its reliance on a limited number of plant species during the sample period. In 2015, only three plant species

(Scytopetalum tieghemii, Dialium aubrevillei, and Calpocalyx brevibracteatus) contributed to the bulk of the diet. Future studies are needed to determine the potential explanations behind such a high degree of selectivity, but my results suggest P. badius badius have a particularly narrow niche breadth. Because specialized species are more likely to be negatively affected by large scale changes in habitat or food availability than are generalist species, such a limited diet has important implications for conservation purposes (Devictor et al. 2008). It is likely that resource specialists with restricted diets will fare poorly as forest structures and phenology patterns continue to change (Devictor et al. 2008, McKinney and Lockwood 1999). Conservation efforts in the Taï Forest would benefit from a comparative study that analyzes the dietary breadths of other resident primate species, including other colobines and cercopithecines. For example,

Scytopetalum tieghemii is clearly a vital tree for the maintenance of viable P. badius badius populations, while other resident primate species may exhibit broader niche breadths and more generalized diets.

Conservation Implications

It has been shown that specialized animals are in a more vulnerable position than generalists when environments change, due to their limited geographic range and heavy reliance on very particular resources. P. badius badius depend on intact forests with high canopies, and species population drastically declines when habitats change rapidly

28

(McGraw 2007). Drops in population due to anthropogenic disturbance or human presence are particularly problematic, because P. badius badius is an endangered primate

(IUCN 2016, Struhsaker 2010) and is considered to be the most vulnerable of all primate species in the Taï Forest due to its particularly high habitat sensitivity, large body size, substrate preference, anti-predatory behavior, and large group size (McGraw 2007). I argue that dietary specialization should be included as another factor in determining a primate’s relative vulnerability. Future studies that identify the dietary breadth of other resident primates in Taï National Park may provide further information about which species are expected to suffer as the forest continues to change.

Major populations of P. badius badius are found in only five locations, of which are all protected areas: Gola Forest Reserves, Outamba-Kilimi National Park, Tiwai

Island Wildlife Sanctuary, Sapo National Park, and Taï National Park (Struhsaker 2010).

The largest and most viable population of P. badius badius is found in Taï National Park, but the population is by no means secure. The most important long term conservation measure is to eliminate poaching across the park (Struhsaker 2010, McGraw 2007); however, dietary analysis of this population provides information for further conservation efforts. As forest compositions continue to change, it will be necessary to predict what consequences are posed to primate diets. In this specific case study, it is clear that there are certain plant species upon which P. badius badius are heavily relying, including

Scytopetalum tiegemii and Dialium aubrevillei. It will be vital to continue monitoring which plant species provide the greatest nutrition and calories for resident primate populations. Forest reserves such as Taï National Park are thought to be the stronghold of

29 future conservation efforts (Struhsaker 2005); therefore, a comprehensive understanding of dietary restrictions and preferences will be vital for maintaining healthy populations.

Analyses of dietary ecology can have implications not only for the population level, but also on larger scales. Several decades of research has revealed an inability to keep any red colobus species in captivity (Struhsaker and Siex 1998, Oates and Davies

1994, Collins and Roberts 1978). Any red colobus species that has been kept in captivity tends to die within a year at best, usually due to gastrointestinal disturbances, nephritis, parasitic infection, or pneumonia (Gijzen et al. 1966, Collins and Roberts 1978). Despite many years of research on feeding ecology of various red colobus species, there remains a clear disconnect between diet and viability in captivity for this taxa. The future of colobine conservation has been argued to rest in the preservation of large, pristine forests

(Struhsaker 2010, McGraw 2007). However, captive breeding and reintroduction for primates has proved to be successful in certain instances, such as the case study of the

Golden Lion Tamarin (Kleinman et al. 1986). Captive breeding and reintroduction programs are certainly controversial, yet they provide a fallback option when wild populations are too small to be self-sustaining. Captive populations can serve as thea repository when a species goes extinct in the wild (Cowlishaw and Dunbar 2000).

Regardless of future conservation methodologies, dietary profiles identify which plant species or nutritional properties are of most importance. It is vital to fully understand the specific nuances of P. badius badius feeding ecology in order to direct future conservation efforts.

30

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Appendix A: Figures

Figure 1: A conceptual model of the niche breadths of specialists (S) and generalists (G) (Photo: Devictor et al. 2010).

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Figure 2: Predicted changes in niche breadths across different locations for specialists (a) and generalists (b) (Photo: Devictor et al. 2010).

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Figure 3: Piliocolobus badius badius in the Taï Forest (Photo: Erin Kane)

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Figure 4: Côte d’Ivoire (Photo: Google Maps)

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Figure 5: A diagram of the TMP study grid and the home ranges of two groups of P. badius badius (Photo: Korstjens 2001).

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Figure 6: Percent contribution to total diet when only the top ten most consumed species are considered in 1996, 1997 and 2015.

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Figure 7: The ripe fruit of Scytopetalum tieghemii

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Figure 8: Scytopetalum tieghemii mature leaves (Photo: Hawthorne and Jongkind 2006)

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Figure 9: Lophira alata mature leaves (Photo: Hawthorne and Jongkind 2006)

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Figure 10: Breakdown of total % contribution of each plant part to the diet in 2015. FU = unripe fruit, BU = unripe buds (closed flowers), LY = young leaves, FR = ripe fruit, LM = mature leaves.

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Figure 11: Comparison of Shannon-Weiner diversity indices for only common species between 1996 and 1997.

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Figure 12: Comparison of Shannon-Weiner indices for only common species between 1997 and 2015.

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Figure 13: Comparison of Shannon-Weiner indices for the Top Ten species between 1996 and 1997.

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Figure 14: Comparison of Shannon-Weiner indices for the Top Ten species between 1997 and 2015.

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Figure 15: Interannual and seasonal variation in phenological scores of mature leaves.

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Figure 16: Interannual and seasonal variation in phenological scores of young leaves.

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Figure 17: Interannual and seasonal variation in phenological scores of unripe fruit.

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Figure 18: Interannual and seasonal variation in phenological scores of ripe fruit.

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Figure 19: Interannual and seasonal variation in phenological scores of open flowers.

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Figure 20: Interannual and seasonal variation in phenological scores of closed flowers.

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Appendix B: Tables

Afrosersalsia afzelii Aningeria robusta Anthonotha fragrans Anthonotha sassandraensis Baphia bancoensis Berlinia grandiflora Bussea occidentalis Calpocalyx brevibact. Canthium multiflorum Chrysophylum taiense Cleistopholis patens Coelocaryon oxicarpum Combretum aphanopet. Coula edulis Craterispermum caudatum Dacryodes klaineana Dialium aubrevillei Diospyros canaliculata Diospyros mannii Diospyros sanza-minika Diospyros soubreana Drypetas aubrevillei Erythrophleum ivorense Gilbertiodendron preussii Heritiera utilis Klainedoxa gabonensis Lophira alata Maesobotria barteri Memecylon lateriflorum Napoleona leonensis Nauclea pobeguini Oldfieldia africana Parinari aubrevillei Parinari excelsa Parinari glabra Parkia bicolor Pentaclethra macrophylla Pentadesma butyracea Piptadeniastrum africanum Pycnanthus angolensis Renoria longicuspis Ricinodendron heudelotii Rinorea longicuspis Sacoglottis gabonensis Samanea dinlagei Scottelia chevalieri Scytopetalum tieghemii Spondianthus preussi Spyropetalum sp. Strephonema pseudocola Syzygium rowlandii Tetracera potatoria Trychoscypha arborea Uapaca esculenta Uapaca guienensis Vitex micrantha Xylopia quintasii Table 1: Plant species included in phenological transects.

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1996 1997 2015 Afrosersalisia 1.52 Acioa scabrifolia 0.18 Anthonota fragrans 1.00 afzelii Aningeria robusta 0.71 Afrosersalisia afzelii 1.11 Berlinia grandiflora 0.11 Anopyxis klaineana 0.06 Agelaea pseudobliqua 0.09 Bri micrantha 1.33 Anthonotha 0.99 Amphimas 0.39 Calpocalyx 13.13 sassaraensis pterocarpoides brevivracteatus Antiaris welwitchii 0.09 Anthonotha fragrans 0.17 Canarium 0.87 schweinfurthii Aphanostylis 0.39 Anthonotha 0.09 Combretum 1.63 leptantha sassaraensis aphanopetalum Baissea species 0.19 Aphanostylis leptantha 0.22 Connarus africanus 2.39 Berlina grandiflora 2.91 Baphia bancoensis 0.22 Coula edulis 0.11 Bombax 0.27 Berlina grandiflora 5.42 Dialium aubrevillei 14.43 buonopozense Bos pho 0.17 Bussea occidentalis 1.25 Erythrophleum 1.67 ivorense Bussea occidentalis 0.77 Caloncoba brevipes 0.34 Garcinia afzelii 0.07 Caloncoba 2.32 Calpocalyx aubrevillei 0.48 Gilbertiodendron 2.84 brevipes preussii Calpocalyx 0.61 Calpocalyx 2.43 Guibourtia ehie 0.43 aubrevillei brevibracteatus Calpocalyx 1.75 Canthium species 0.08 Heritiera utilis 0.53 brevibracteatus Canthium species 0.11 Carapa procera 0.77 Irvingia gabonensis 0.33 Carapa procera 0.06 Cola gigantean 0.04 Klainedoxa 0.97 gabonensis Cola gigantean 0.30 Combretodendron 0.29 Lannea welwitschii 0.46 africanum Combretodendron 0.03 Combretum 2.96 Lophira alata 2.51 africanum aphanopetalum Combretum 2.72 Coula edulis 2.87 Oldfieldia africana 0.99 aphanopetalum Combretum species 0.06 Dacryodes klaineana 1.17 Pachypodanthium 0.31 staudtii Connarus 0.05 Detarium senegalense 0.18 Panda oleosa 0.43 africanus Copaifera 0.16 Dialium aubrevillei 6.35 Parkia bicolour 0.26 salikounda Continued Table 2: All tree species consumed and percent contribution to diet in 1996, 1997, and 2015. 60

Table 2 Continued

Coula edulis 4.24 Diospyros sanza- 3.13 Parinari glabra 0.19 minika Dacryodes 1.24 Diospyros soubreana 0.39 Pentadesma 0.54 klaineana butyracea Detarium 0.16 Distemonanthus 0.25 Pentaclethra 2.26 senegalense benthamianus macrophylla Dialium dinklagei 0.22 Drypetes gilgiana 0.04 Piptadeniastrum 2.33 africanum Diospyros 0.04 Enantia polycarpa 0.04 Polyalthia oliveri 0.13 canaliculata Diospyros mannii 0.02 Erythrophleum 1.27 Scytopetalum 38.39 ivorense tieghemii Diospyros sanza- 2.83 Ficus eriobotryoides 0.04 Spondianthus 0.23 minika preussi Diospyros 0.16 Ficus lyrata 0.13 Syzygium rowlandii 6.31 soubreana Enantia polycarpa 0.19 Ficus sagittifolia 0.19 Tetracera potatoria 1.42 Erythrophleum 1.99 Ficus species 0.09 Uapaca esculenta 1.09 ivorense Ficus 0.03 Garcinia afzelii 1.36 Xylopia quintasii 0.19 eriobotryoides Ficus 0.52 Gilbertiodendron 7.65 Xylopia villosum 0.21 macrosperma preussii Ficus species 0.20 Irvingia gabonensis 2.40 Funtumia africana 0.30 Klainedoxa gabonensis 1.24 Garcinia afzelii 0.93 Landolphia blique 0.14 Gilbertiodendron 1.23 Lannea welwitschii 0.13 preussii Heritiera utilis 1.29 Liana species 0.04 Irvingia 1.96 Lophira alata 7.33 gabonensis Irvingia 0.06 Manniophyton fulvum 0.38 grandiflora Klainedoxa 4.38 Memecylon 0.50 gabonensis lateriflorum Landolphia hirsute 0.65 Nauclea diderrichii 0.04 Leptoderris species 0.05 Nauclea pobequinii 0.84 Liana species 0.08 Newtonia 0.41 duparquatiana Linocierra nilotica 0.05 Oldfieldia africana 0.87 Continued 61

Table 2 Continued Lophira alata 8.62 Ongokea gore 0.34

Lovoa trichilioides 0.07 Pachypodanthium 0.26 staudtii Macaranga barteri 0.17 Parinari aubrevillei 0.76 Mammea africana 1.76 Parinari excelsa 0.00 Memecylon afszelii 0.15 Parinari glabra 1.76 Mitragyna ciliata 0.10 Parkia bicolour 2.49 Nauclea diderrichii 0.17 Pentaclethra 1.10 macrophylla Nauclea pobeguinii 0.23 Pentadesma butyracea 0.84 Nes pap 0.03 Piptadeniastrum 2.45 africanum Oldfieldia africana 0.98 Ricinodendron 2.77 heudelotii Ongokea gore 0.61 Rinorea longiscuspis 0.09 Pachypodanthium 0.75 Samanea dinklagei 0.73 staudtii Panda oleosa 0.40 Scytopetalum tieghemii 22.09 Parinari 1.46 Spondianthus preussii 0.17 aubrevillei Parinari excelsa 0.22 Strephonema 0.87 pseudocala Parinari glabra 4.39 Strombosia 1.45 glaucescens Parkia bicolour 1.65 Syzygium rowlandii 0.89 Pentaclethra 1.99 Tarretia utilis 0.23 macrophylla Pentadesma 0.76 Tetrapleura chealieri 0.13 butyracea Piptadeniastrum 0.77 Trichilia martineaui 0.35 africanum Ricinodendron 4.96 Trichoscypha arborea 0.17 heudelotii Rinorea 0.11 Tristemma coronatium 0.22 longiscuspis Sacoglottis 0.02 Uapaca esculenta 2.16 gabonensis Scottelia chevalieri 0.80 Uapaca guineensis 0.25 Scottelia coriacea 0.15 Unknown 0.57 Continued

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Table 2 Continued Scytopetalum 18.36 Vitex rivularis 0.42 tieghemii Spondianthus 0.99 Xylopia aethiopica 0.09 preussii Sterculia oblonga 0.03 Xylopia parviflora 0.08 Strephonema 0.90 Xylopia quintasii 0.21 pseudocala Strombosia 1.04 Xylopia villosum 0.07 glaucescens Symphonia 0.20 globulifera Tristemma 0.12 coronatum Uapaca esculenta 6.30 Uapaca guineensis 0.38 Uapaca paludosa 0.06 Unknown 0.22 Vitex rivularis 0.45 Xylopia quintasii 0.54

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1996 1997 2015 Scytopetalum Scytopetalum Scytopetalum 18.36 22.09 38.39 tieghemii tieghemii tieghemii Gilbertiodendron Lophira alata 8.62 7.65 Dialium aubrevillei 14.43 preussii Calpocalyx Uapaca esculenta 6.30 Lophira alata 7.33 13.13 brevibracteatus Ricinodendron 4.96 Dialium aubrevillei 6.35 Syzygium rowlandii 6.31 heudelotii Gilbertiodendron Parinari glabra 4.39 Berlina grandiflora 5.42 2.84 preussii Klainedoxa Diospyros sanza- 4.38 3.13 Lophira alata 2.51 gabonensis minika Combretum Coula edulis 4.24 2.96 Connarus africanus 2.39 aphanopetalum Piptadeniastrum Berlina grandiflora 2.91 Coula edulis 2.87 2.33 africanum Diospyros sanza- Ricinodendron Pentaclethra 2.83 2.77 2.26 minika heudelotii macrophylla Combretum Erythrophleum 2.72 Parkia bicolour 2.49 1.67 aphanopetalum ivorense Table 3: The top ten most consumed plant species and their total percent contribution to dietary profiles for 1996, 1997, and 2015.

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Tree Species 1996 1997 2015 Berlinia grandiflora 2.91 5.42 0.11 Calpocalyx brevivracteatus 1.75 2.43 13.13 Combretum aphanopetalum 2.72 2.96 1.63 Coula edulis 4.24 2.87 0.11 Erythrophleum ivorense 1.99 1.27 1.67 Garcinia afzelii 0.93 1.36 0.07 Gilbertiodendron perussi 1.23 7.65 2.84 Irvingia gabonensis 1.96 2.40 0.33 Klainedoxa gabonensis 4.38 1.24 0.97 Lophira alata 8.62 7.33 2.51 Oldfieldia africana 0.98 0.87 0.99 Pachypodanthium staudtii 0.75 0.26 0.31 Parinari glabra 4.39 1.76 0.19 Parkia bicolour 1.65 2.49 0.26 Pentaclethra macrophylla 1.99 1.10 2.26 Pentadesma butyracea 0.76 0.84 0.54 Piptadeniastrum africanum 0.77 2.45 2.33 Scytopetalum tieghemii 18.36 22.09 38.39 Spondianthus preussi 0.99 0.17 0.23 Uapaca esculenta 6.30 2.16 1.09 Xylopia quintasii 0.54 0.21 0.19 Table 4: The percent contribution to diet of plant species consumed in all three sample periods.

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% Contribution Food Item to Total Diet Ripe Fruit 3.11 Unripe Fruit 37.78 Mature Leaves 1.00 Young Leaves 27.33 Young Flower Buds 30.56 Table 5: Percent composition of the diet expressed as food items consumed during the 2015 sample period.

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Year H EH All Species

1996 3.437 0.778 1997 3.285 0.761 2015 2.195 0.628 Only Conserved Species

1996 2.557 0.840 1997 2.433 0.799 2015 1.662 0.546 Only Top Ten Species

1996 2.089 0.908 1997 2.014 0.874 2015 1.805 0.784 Table 6: Shannon-Wiener indices of diversity (H) and Evenness scores (EH) for every year in three different comparisons.

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Table 7: Average monthly and annual phenology scores for mature leaves, young leaves, unripe fruit, ripe fruit, open flowers, closed flowers.

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LM LY FR FU FlC FlO 2006 2.96 0.03 0.05 0.11 0.03 0.05 2009 2.96 0.02 0.06 0.15 0.03 0.08 2014 2.98 0.01 0.09 0.11 0.04 0.03 r 0.982 -0.989 0.99 -0.143 0.929 -0.524 p 0.43 0.09 0.08 0.909 0.243 0.648 Table 8: Mean annual phenological scores and Pearson’s Correlation Coefficient and p- Values for each plant part. LM = mature leaves, LY = young leaves, FR = ripe fruit, FU = unripe fruit, FlC = closed flowers, and FlO = open flowers.

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LM LY FR FU FlC FlO 2006 3.00 0.00 0.00 0.00 0.00 0.06 1009 3.00 0.00 0.00 0.00 0.03 0.06 2014 3.00 0.00 0.00 0.00 0.30 0.00 r n/a n/a n/a n/a 0.93 -0.93 p n/a n/a n/a n/a 0.24 0.24 Table 9: Mean annual phenological scores and Pearson’s Correlation Coefficient and p- Values for each plant part for Scytopetalum tiegemii. LM = mature leaves, LY = young leaves, FR = ripe fruit, FrU = unripe fruit, FlC = closed flowers, and FlO = open flowers.

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LM LY FR FU FlC FlO 2006 2.74 0.26 0.00 0.00 0.00 0.00 1009 2.90 0.10 0.00 0.00 0.00 0.00 2014 2.78 2.02 1.80 1.80 1.80 1.80 r 0.099 0.898 0.929 0.929 0.929 0.929 p 0.937 0.290 0.243 0.240 0.240 0.240 Table 10: Mean annual phenological scores and Pearson’s Correlation Coefficient and p- Values for each plant part for Lophira alata. LM = mature leaves, LY = young leaves, FR = ripe fruit, FU = unripe fruit, FlC = closed flowers, and FlO = open flowers.

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