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Effects of human disturbance on primate dynamics

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Effects of human disturbance on primate dynamics
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Gillespie, Thomas R
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Ecology ( jstor )
Environmental conservation ( jstor )
Forests ( jstor )
Infections ( jstor )
Logging ( jstor )
Monkeys ( jstor )
National parks ( jstor )
Parasites ( jstor )
Primates ( jstor )
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Dissertations, Academic -- Zoology -- UF
Zoology thesis, Ph. D
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Thesis (Ph. D.)--University of Florida, 2004.
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Includes bibliographical references.
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Vita.
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by Thomas R. Gillespie.

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EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS


By

THOMAS R. GILLESPIE

















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


2004






























Copyright 2004

by

Thomas R. Gillespie














ACKNOWLEDGMENTS

I thank my advisor, Colin Chapman, whose support and assistance were invaluable during this work. His expertise and enthusiasm provided a solid foundation for this study. I owe much to my committee members (Drs. Sue Boinski, Lauren Chapman, Ellis Greiner, and Michael Huffmnan) for their advice and support throughout this venture. Drs. Andy Dobson, Donald Forrester, Robert Holt, William Karesh, Joanna Lambert, Arthur Mugisha, Thomas Struhsaker, and the honorable Betty Udongo shared insights that improved this work.

I am grateful to Dennis Sebugwawo and all employees of the Kibale Fish and

Monkey Project for their hard work and dedication. I am grateful to Stacey Bonovitch, Lauren Castleberry, Brian Davidson, John Davis, Jennifer Davis-Summer, Erin Ehmke, Kristen Guttmann, Sarah Hawkins, Joe Mahoney, Anjan Patel, Michelle Roman, May Stewart, Gregory Zhelesnik, and Jennifer Zipser for their assistance in the laboratory. I thank my many colleagues at Kibale National Park, Uganda, and the University of Florida who have shared insight, advice, friendship, and humor. Especially Evelina Jagminaite who saw me through much of this work.

I am ever grateful to my parents, Robert and Margaret Gillespie, who have been a constant source of encouragement and support throughout my life.

This research has been supported by grants from the National Center for

Environmental Research of the United States Environmental Protection Agency (STAR Fellowship), the National Science Foundation (grant number SBR-990899), the Wildlife








Conservation Society, and the Ford Foundation. Permission to conduct this research was provided by the Uganda National Research Council, Office of the President, the Uganda Wildlife Authority, and Makerere University.

This dissertation is dedicated to Brian Riewald, whose spirit and character will always be with me.















TABLE OF CONTENTS
Page

ACKN OW LED GM EN TS ................................................................................................ iii

LIST OF TABLES..........................................................................................................viii

LIST OF FIGURES ........................................................................................................... x

ABSTRACT....................................................................................................................... xi

CHAPTER

1 INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE
DYN AM ICS ................................................................................................................1

Overview ....................................................................................................................... 1
Hum an D isturbance and Prim ate Populations .............................................................2
Prim ate-Parasite D ynam ics..........................................................................................5
D isturbance and Prim ate-Parasite D ynam ics...............................................................6
Rationale.......................................................................................................................8

2 GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN
U GAND A ................................................................................................................10

Introduction.................................................................................................................10
M aterials and M ethods ..............................................................................................11
Results.........................................................................................................................12
N em atoda............................................................................................................12
Cestoda................................................................................................................14
Trem atoda...........................................................................................................14
Protozoa..............................................................................................................15
Effect of Season and Host Sex on Infection Prevalence ....................................15
Variation in Prevalence among Sites throughout Africa....................................15
D iscussion...................................................................................................................16

3 GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF
U GAN D A ................................................................................................................... 21

Introduction................................................................................................................. 21
M aterials and M ethods ........................................................................ . 22
Results......................................................................................................................... 23









N em atoda............................................................................................................23
Cestoda...............................................................................................................25
Trem atoda.........................................................................................................26
Protozoa...............................................................................................................26
Effect of Season and Host Sex on Infection Prevalence ....................................27
D iscussion...................................................................................................................27

4 LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN
AFRICAN PRIM A TE POPU LA TION S...................................................................32

Introduction.................................................................................................................32
M aterials and M ethods ..............................................................................................35
Study Site............................................................................................................35
Fecal Sam pling and Analysis .............................................................................37
Infection Risk A ssessm ent .................................................................................38
Statistical A nalyses............................................................................................39
Results.........................................................................................................................39
Infection Prevalence and Richness.....................................................................39
Infection Risk .....................................................................................................40
D iscussion.................................................................................................................40

5 ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES
IN FOREST FRA G M EN TS ..................................................................................... 53

Introduction.................................................................................................................53
M aterials and M ethods ..............................................................................................55
Study Site............................................................................................................55
Fecal Sam pling and A nalysis .............................................................................55
Infection Risk A ssessm ent .................................................................................56
Colobus Surveys.................................................................................................57
Statistical A nalyses.............................................................................................57
Results.........................................................................................................................57
Infection Prevalence and Richness.....................................................................57
Infection Risk .....................................................................................................58
Colobus Population D ynam ics ...........................................................................58
D iscussion...................................................................................................................59

6 VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST
FRA G M EN T A TTRIBU TES..................................................................................... 67

Introduction.................................................................. ............................................... 67
M aterials and M ethods ............................................................................................... 70
Study Site .................................................. ........................... 70
Fecal Sam pling and Analysis .............................................................................70
Infection Risk A ssessm ent .................................................................................71
Fragm ent Characteristics....................................................................................71



vi









Results.........................................................................................................................73
Discussion...................................................................................................................75

7 SUM M ARY AND CON CLU SION S ........................................................................80

LIST OF REFEREN CES................................................................................................... 82

BIOGRAPH ICA L SKETCH ............................................................................................ 99














LIST OF TABLES


Table page

2-1 Prevalence (%) of gastrointestinal helminth parasite infections in guenons of
w estern U ganda ....................................................................................................... 19

3-1 Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys
of U ganda .................................................................................................................30

4-1 Mode of infection, morbidity, and mortality associated with gastrointestinal
parasites infecting redtail guenon (Cercopithecus ascanius), red colobus
(Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda...........................48

4-2 Prevalence (%) of gastrointestinal parasite infections in redtail guenons
(Cercopithecus ascanius) from logged and undisturbed forests in Kibale National
P ark, U ganda ........................................................................................................... 49

4-3 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from logged and undisturbed forests in Kibale National Park, Uganda50

4-4 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from logged and undisturbed forests in Kibale National Park,
U gan da .....................................................................................................................5 1

5-1 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from forest fragments and undisturbed forests in Kibale National Park, U gan da ....................................................................................................................63

5-2 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from forest fragments and undisturbed forests in Kibale
N ational Park, U ganda ............................................................................................64

6-1 Physical and biological attributes of forest fragments with red colobus
(Piliocolobus tephroceles) populations near Kibale National Park, Uganda...........77

6-2 Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus
monkeys (Piliocolobus tephroceles) in forest fragments near Kibale National Park, U ganda ....................................................................................................................78








6-3 Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus
monkeys (Piliocolobus tephrosceles) and attributes of the forest fragments they
inhabit near Kibale National Park, Uganda.............................................................79














LIST OF FIGURES


Figure page

2-1 Inter-monthly variation in parasite infection prevalence of redtail guenons and
rainfall at Kibale National Park, Uganda ................................................................20

3-1 Inter-monthly variation in parasite infection prevalence of colobus monkeys and
rainfall at Kibale National Park, Uganda ................................................................31

4-1 Mean number of parasite species infecting individual redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-andwhite colobus (Colobus guereza) in undisturbed and logged forest at Kibale
N ational Park, U ganda ............................................................................................52

5-1 Conceptual model of proposed mechanism for population declines in forest .........65

5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus
tephrosceles), and black-and-white colobus (Colobus guereza) in undisturbed and
fragm ented forest W estern Uganda.........................................................................66














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

EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS By

Thomas R. Gillespie

August 2004

Chair: Colin A. Chapman
Major Department: Zoology

Emerging infectious diseases have raised global awareness of the impact ecological change can have on biodiversity conservation and wildlife and human health. This study improves our understanding of this interplay by examining effects of logging and forest fragmentation on parasite dynamics in an African primate community. From August 1997 to July 2003, 2,017 fecal samples were collected to compare gastrointestinal parasite infections of red colobus (Piliocolobus tephroceles), black-and-white colobus (Colobus guereza), and redtail guenon (Cercopithecus ascanius) populations from logged (all), fragmented (only colobines), and undisturbed forests (all) at Kibale National Park, Uganda. Dynamics of red colobus infection with strongyle and rhabditoid nematodes were examined in relation to forest fragment attributes. Helminth eggs, larvae, and protozoan cysts were identified using sodium-nitrate flotation and fecal sedimentation. Coprocultures and necropsies facilitated identification. Infection-risk was quantified by modified sedimentation technique, comparing densities of infective-stage parasites from canopy and ground vegetation plots in logged, fragmented, and undisturbed forest.








Prevalence and richness of gastrointestinal parasite infections and magnitude of multiple infections were greater for guenons in logged than in undisturbed forest, but these parameters did not differ between forest types for either colobine. Infection-risk was greater for primates in logged compared to undisturbed forest. Prevalence and richness of gastrointestinal helminth and protozoan parasite infections and frequency of multiple infections were greater for red colobus in fragmented than in undisturbed forest, but these parameters did not differ between these areas for black-and-white colobus. Infection-risk was greater for colobines in fragmented compared to undisturbed forest. Inter-fragment comparisons examining 10 potential factors demonstrated that an index of degradation, tree-stump-density, strongly influenced prevalence of strongyle and rhabditoid nematodes. Infection risk was also higher in the fragment with highest stumpdensity compared to the fragment with lowest stump-density. Fragment size and colobine density were correlated to prevalence for some nematodes, but in multiple regression analyses with stump-density, these variable did not explain a significant amount of variance.

These results demonstrate that selective logging and forest fragmentation have the capacity to affect parasite infection dynamics in some African primate species. These changes in infection dynamics may play a role in observed primate declines.













CHAPTER 1
INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE DYNAMICS

Overview

Tropical forests, although covering only 6% of Earth's arable surface, account for nearly 50% of all known species (National Research Council 1992). Less than 5% of tropical forests are legally protected (Redford 1992; Oates 1996; Chapman et al. 2000) and unprotected forests are being degraded at staggering rates (FAO 1999; Chapman and Peres 2001). Consequently, conservation of many tropical forest species (such as primates) will depend, at least in part, on the capacity of disturbed areas outside of reserves to support their populations.

Ninety percent of primate species are restricted to the tropics (Mittermeier and Cheney 1987), and more than half of primate species are threatened by extinction (Chapman and Peres 2001). Thus, primates represent an ideal taxa for studying the effects of human disturbance in tropical forests. Although human disturbance is known to negatively impact primate populations, little is known about the mechanisms responsible for such effects. One such mechanism may be infection dynamics.

Emerging tropical diseases (such as AIDS and Ebola) have raised global awareness of the strong linkage between biodiversity conservation and the health of animal and human populations (Meffe 1999; Daszak et al. 2000, 2001). To effectively understand the dynamics of emerging diseases, we must evaluate the interplay among alteration and fragmentation of tropical forests, wildlife-human disease linkages, and the ecology of








novel diseases. My study addresses an important aspect of these questions by examining the effects of selective logging and forest fragmentation on primate-parasite dynamics in an African tropical forest.

To provide background information on the framework of the research, this

introduction reviews the patterns of human disturbance and their impacts on primate populations. Little is known about the mechanisms by which human disturbance impacts primate populations and ecosystem processes. My study examines one potential mechanism, primate-parasite dynamics. Since it is likely that pathogens and other factors interact to produce an effect on primate populations, I provide background on human disturbance and primate populations, and discuss how this may relate to primate-parasite dynamics. This is followed by the objectives, rationale, methodology, and research implications of my work.

Human Disturbance and Primate Populations

Forest fragmentation and selective logging dominate habitat-modification patterns throughout the tropics (Chapman et al. 2000; Chapman and Peres 2001) and have detrimental effects on most primate populations (Skorupa 1988; Bierregaard et al. 1992; Bennett and Dahaban 1995; Chapman et al. 2000; Onderdonk and Chapman 2000). With respect to forest fragmentation, primate species richness is lower in forest fragments compared to equivalent areas of continuous forest (Bierregaard et al. 1992; Onderdonk and Chapman 2000); primate species richness is typically higher in large compared to small fragments (Bierregaard et al. 1992; Estrada et al. 1994; but see Onderdonk and Chapman 2000); and primate densities typically are higher in large compared to small fragments (Estrada and Coates-Estrada 1996; Chiarello 2000; but see Onderdonk and








Chapman 2000). Thus, forest fragmentation appears to negatively impact most primate communities and species.

The impact of selective logging on primate populations depends greatly on the intensity of the logging and the species in question. Low-intensity logging (5-20% of trees destroyed) appears to be compatible with primate conservation (Johns and Skorupa 1987; Ganzhorn 1995; Oates 1996; Brugiere 1998; Chapman et al. 2000). For example, Ganzhom (1995) determined that low-intensity logging of forests in Madagascar (affecting less than 10% of forest area) corresponds with an increase in abundance of all lemur species (significantly so for three of seven species). Moreover, studies from Kibale National Park in Uganda demonstrate that primate densities in low-intensity logged forest are no different from primate densities in unlogged forest (Skorupa 1988; Chapman et al. 2000). Consequently, low-intensity, selective logging potentially offers a land-use option compatible with primate conservation.

In contrast, high-intensity logging (>50% of trees destroyed), the most common form of logging in the tropics, appears to be detrimental to most primate populations (Skorupa 1988; Bennett and Dahaban 1995; Chapman et al. 2000). For example, Bennett and Dahaban (1995) found that high-intensity logging resulted in a 35-70% decline in gibbon (Hylobates muelleri) and langur (Presbytis sp.) populations in Sarawak. Skorupa (1988) demonstrated that 12 years after high-intensity logging, group densities of red colobus (Piliocolobus tephrosceles) and red-tail guenons (Cercopithecus ascanius) were lower compared to those in unlogged forest at Kibale National Park, Uganda. Chapman et al. (2000) reveals that even 28 years after logging in the system examined by Skorupa (1988), red-tail group densities were still lower in high-intensity logged forest compared








to unlogged forest. Moreover, group densities of Cercopithecus ascanius and C mitis in high-intensity logged forest continued to decline even 28 years after logging (Chapman et al. 2000). In contrast, the density of eastern black-and-white colobus (Colobus guereza) was not lower in logged compared to undisturbed forest at both 12 and 28 years after logging (Skorupa 1988, Chapman et al. 2000). Thus, although some primate species may cope well with high-intensity selective logging, the majority of primates fair poorly.

Although forest fragmentation and high-intensity, selective logging are known to negatively impact primate abundance and species richness, little is known about the proximate mechanisms responsible for such effects. To successfully combat species loss in such systems, we must understand the underlying mechanisms of species loss. Parasite dynamics may be one such mechanism.

Animal populations are largely regulated by three factors: availability of quality food, predation, and infectious disease (Lack 1954; Minchella and Scott 1991; Dobson 1995). While a great deal of research has focused on the effects of food availability and predation on primate abundance (Struhsaker 1976; Milton 1982; Isbell 1990; Struhsaker and Leaky 1990; Chapman and Chapman 1999), the role of infectious disease has remained largely unexplored (Stuart and Strier 1995). Forest fragmentation and highintensity, selective logging may alter primate-parasite dynamics (resulting in higher rates of primate mortality, lower reproductive rates, and debilitation). Consequently, an understanding of how these manifestations of human disturbance affect primate-parasite dynamics could be of central importance in designing effective conservation and management plans.








Primate-Parasite Dynamics

Gastrointestinal parasites infecting mammals are commonly transmitted through contact with the free-living stages, ova, or larvae. This may involve contact with contaminated food, water, fecal material, or soil (with vertebrate or invertebrate vectors), or may involve direct contact with infected individuals (Brown and Neva 1983). Parasites impact host survival and reproduction directly through pathological effects, and indirectly by reducing host condition (Chandra and Newberne 1977; Hart 1988, 1990, 1992; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Despommier et al. 1995; Coop and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous abortion, congenital malformations, and death (Chandra and Newberne 1977; Despommier et al. 1995). Less severe infections may impair nutrition; may increase energy expenditure; or may impair travel, feeding, escape from predators, and competition for resources or mates (resulting in mortality or lower fitness) (Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996; Hart 1988, 1990, 1992). Through these proximate mechanisms, parasites can ultimately regulate host populations (Gregory and Hudson 2000; Hochachka and Dhondt 2000) or cause shortterm reductions in population size (Collias and Southwick 1952; Work et al. 1957).

Few studies have investigated the effects of parasite infections on wild primate populations. However, evidence suggests that parasite infections can lead to primate mortality. For example, Ohsawa (1979) and Dunbar (1980) demonstrated that larval cestode infections contributed to high mortality rates for immature and older gelada baboons (Theropithecus gelada). Several studies have demonstrated endoparasitic, ectoparasitic, and viral epidemics in great ape populations in areas near human settlement (Ashford et al. 1990; Hastings et al 1991; Kortlandt 1996; Meader et al. 1997; Pussey








1998). Each of these epidemics was potentially anthropozoonotic, meaning that the apes were potentially infected by contact with humans. Yellow fever was implicated as the cause of a 50% decline in the howling monkey (Alouatta palliata) population on Barro Colorado Island, Panama, between 1933 and 1951 (Collias and Southwick 1952). Later studies of this same howling monkey population suggested that heavy botfly infestations (Alouattamyia baeri), in conjunction with food limitation, were limiting monkey densities (Smith 1977; Milton 1996). Interestingly, Barro Colorado Island was isolated from a much larger area of continuous disturbed forest after the damming of Lake Gatun during the formation of the Panama Canal, and is hence the result of large-scale human disturbance. The predominance of cases of population-level effects of parasites on primates from human-disturbed systems suggests that populations in disturbed habitats may be more vulnerable to parasites. However, more studies will be needed to confirm this, since few studies have expressly looked at such issues in undisturbed systems.

Disturbance and Primate-Parasite Dynamics

The direct pathological effects and accompanying reduction in host condition resulting from parasitic infections may play a role in the lower abundance and species richness of primate communities in disturbed systems. While reproductively active primate groups may be sustained in forest fragments and selectively logged forests, little is known about the effects of such disturbance on primate health. These disturbance regimes result in changes in forest structure and climate, increased human presence, and decreased food availability (Kapos 1989; Williams-Linera 1990; Laurance et al. 1996; Didham and Lawton 1999; Chapman et al. 2000; Chapman and Peres 2001). Such changes may increase or decrease the likelihood of parasite infection. Forest fragments have consistently lower canopy height and higher foliage density than continuous forest








(Williams-Linera 1990; Camargo 1993; Malcolm 1994; Laurance et al. 1996). Higher foliage density has also been demonstrated for selectively logged forests (Ganzhorn 1995). Lower canopy height may increase overlap in arboreal pathways among primates and higher foliage density may increase the surface area exposed to falling feces. Consequently, these characters may increase the probability of contact with infected fecal material for primates. However, microclimatic change resulting from disturbance may negatively influence the lifecycle of a parasite (Stuart et al. 1993). Forest fragments maintain higher temperature and higher rates of evaporative drying compared to continuous forest (Kapos 1989; Laurance et al. 1996; Didham and Lawton 1999). Such abiotic conditions may result in shorter survival time for free-living larvae within fecal material because of rapid desiccation (Meade 1983).

Forest fragmentation and selective logging are often accompanied by increased contact between primates and humans. Primates act as reservoirs for human pathogens and likewise, humans act as reservoirs for diseases to which other primates are susceptible (Lopez-Neyra 1949; Brown and Neva 1983; Meade 1983; Horii and Usui 1985; Stuart et al. 1990; Wolfe et al. 1998). With increased population densities of humans and inflated densities of primates in fragmented habitats, the probability of contact with infectious fecal material and infected hosts increases. Thus, increased contact with humans may increase infection risk for primates in forest fragments and selectively logged forests.

In forest fragments, primate densities may be high because of immigration from cleared areas (Onderdonk and Chapman 2000). Thus, groups there often have more restricted, overlapping ranges than do groups in continuous forest. Crowding and re-use








of restricted areas may increase the probability of a primate coming into contact with an infected individual or areas contaminated with infectious fecal material. For example, chimpanzees (Pan troglodytes) and howling monkeys (Alouatta palliata and A. seniculus) demonstrate higher prevalence of parasite infections in groups with restricted ranges or in groups at higher population density (McGrew et al. 1989; Stuart et al. 1990; Gilbert 1994). Gilbert (1994) also demonstrated that prevalence of endoparasitic infection was positively correlated with the density of sympatric primate species. Thus, crowding resulting from forest fragmentation may increase transmission of infectious parasites among primates.

If there is a reduction of food availability associated with forest fragmentation or selective logging, this may result in decreased animal condition. Reductions in animal condition due to food stress can increase vulnerability to disease or parasites, resulting in population declines (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). Thus, it appears likely that human disturbance, such as forest fragmentation and high-intensity, selective logging may alter the risk of parasite infection for primates.

Rationale

My objective was to determine the consequences of various forms of human

disturbance (including selective logging and forest fragmentation) on primate-parasite dynamics. To meet this objective, I intensively surveyed the primate community of Kibale National Park and surrounding areas to determine prevalence and diversity of gastrointestinal parasites. Chapter 2 presents the findings of these surveys for the guenon species. Chapter 3 presents the findings of these surveys for the colobine species. Next, I compared infection dynamics for red colobus, black-and-white colobus, and redtail guenons between selectively logged forest and undisturbed forest. Details of this aspect





9


of the study are presented in Chapter 4. I made a similar comparison, examining infection dynamics for red colobus and black-and-white colobus between forest fragments and undisturbed forest. Details of this aspect of the study are presented in Chapter 5. Finally, I examined the relationship among physical and biological attributes of forest fragments and strongyle nematode infection dynamics in red colobus. Details of this aspect of the study are presented in Chapter 6.













CHAPTER 2
GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN UGANDA Introduction

The guenons, Cercopithecus spp., are the most diverse taxa of primates endemic to sub-Saharan Africa (Grubb et al. 2002). These frugivorous monkeys live in groups of 1030 individuals and often form mixed-species associations with other primate species (Chapman and Chapman 2000). Although guenons can be found in a wide variety of habitats, the majority inhabit tropical forests (Butynski 2002). More than two-thirds of sub-Saharan Africa's original forest cover has been lost because of anthropogenic disturbance (World Resources Institute 1998), and forest cover continues to decline at a rate of 0.7% annually (FAO 1999). Due largely to resultant habitat loss, 26% of guenons are endangered (Butynski 2002).

Although parasite infections are common in nature and low-intensity infections are often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic change may result in a loss of stability associated with altered transmission rates, host range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline data on patterns of parasitic infections in wild guenon populations are critical to provide an index of population health, and to begin to assess and manage disease risks.

Although many studies have documented the gastrointestinal parasites of wild

populations of African apes (Huffman et al. 1997; Graczyk et al. 1999; Nizeyi et al. 1999; Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et al. 1989; Mtiller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other








African primate taxa remain poorly known. The present study identifies and quantifies the gastrointestinal helminth parasites for the 4 guenon species of western Uganda: redtail guenons (Cercopithecus ascanius), blue monkeys (C. mitis), l'hoesti monkeys (C. lhoesti), and vervet monkeys (C. aethiops). For the most common species (the redtail guenon), I also report protozoan parasites, and examine the effect of season and host sex on parasite prevalence.

Materials and Methods

From January 1998 to December 2002, I collected 293 fecal samples from freeranging guenons at forested sites in western Uganda; 235 from redtail guenons, 35 from blue monkeys, 11 from l'hoesti monkeys, and 12 from vervet monkeys. Samples from redtail guenons, blue monkeys, and l'hoesti monkeys were collected in Kanyawara, a 1,034 ha area characterized by logged and unlogged forest within Kibale National Park (766 km2; 0013'-0041' N, 30019'-30032' E; Struhsaker 1997). Samples from vervet monkeys were collected at Lake Saka, a forest fragment 30 km northwest of the national park. The region experiences a bimodal pattern of seasonal rainfall, with peaks occurring in March-May and August-November (Figure 2-1). Mean annual rainfall (1990-2001) is 1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged 14.90C and 20.20C, respectively, from 1990 to 2001.

Samples were collected immediately after defecation to avoid contamination, and were examined macroscopically for adult nematodes and tapeworm proglottids. With the exception of redtail guenons, samples represent individuals. In the case of redtail guenons, samples are the result of repeated collections from approximately 150 animals. Samples were stored individually in 5.0-mL sterile vials in 10% neutral formalin solution. Preserved samples were transported to the University of Florida, where they were








examined for helminth eggs and larvae, and protozoan cysts, using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Parasites were identified on the basis of egg or cyst color, shape, contents, and size. Iodine was used to facilitate protozoan identification. Measurements were made to the nearest 0.1 i SD, using an ocular micrometer fitted to a compound microscope; and representatives were photographed. Mean egg sizes presented are based on measurement of 10 eggs from 10 different hosts unless otherwise noted. Coprocultures (10 per guenon species except vervets), were used to match parasite eggs to larvae for positive identification of strongylate nematodes (MAFF 1979). Our capacity to identify most parasite species from host fecal examination, even with cultured larvae, is limited. Thus, I present most of my findings at the level of family or genus.

I performed chi-square tests of independence to compare the prevalence of

infections between redtail guenons and blue monkeys. Small sample size precluded me from including l'hoesti and vervet monkeys in these comparisons. Chi-square tests of independence were also performed to compare prevalence between host sex for redtail guenons, and to compare prevalence for the blue monkey population to previously published reports. I used Pearson correlations to test for relationships between monthly rainfall and prevalence of parasites infecting redtail guenons.

Results

Nematoda

Trichuroidea: Trichuris sp. was identified based on egg size and morphology

(barrel-shape, yellow-brown coloration, and bipolar plugs). Eggs were found in feces of all guenon species, and measured 55.1 + 1.2 X 27.2 + 1.1 gm for redtail guenons, 60.0 2.0 X 27.0 1.4 gm for blue monkeys, 58.3 + 1.2 X 27.1 1.1 gm for l'hoesti monkeys,








and 57.9 + 1.4 X 26.7 + 1.6 am for vervets. Prevalence of infection with Trichuris sp. did not differ between redtail guenons (30%) and blue monkeys (26%) (P > 0.05, Table 2-1).

Strongyloidea: Oesophagostomum sp. was identified on the basis of egg size and morphology (elliptical, unlarvated) and cultured larvae. Eggs were found in feces of all guenon species except vervets, and measured 69.1 + 1.8 X 42.4 2.0 Am for redtail guenons, 70.5 + 2.0 X 41.3 + 1.7 Am for blue monkeys, and 73.1 + 1.2 X 43.0 + 1.4 Am for l'hoesti monkeys. Prevalence of Oesophagostomum sp. did not differ (P > 0.05) between redtail guenons (10%) and blue monkeys (9%) (Table 2-1). Unidentified strongyle eggs were found in vervet feces (42%) and measured 72-52 X 42-35 Jim. These strongyles may represent Nectator sp., Ancylostoma sp., and/or Oesophagostomum sp.; however, coprocultures were not performed, limiting our ability to identify these parasites.

Rhabditoidea: Strongyloidesfulleborni was identified based on egg size and

morphology (oval, thin-shelled, colorless, larvated) and verified by cultured rhabditiform larvae. Eggs were found in feces of all guenon species, and measured 50.2 + 2.3 X 33.7 4.1 jm for redtail guenons, 43.7 5.0 X 35.4 + 3.1 jm for blue monkeys, 46.5 3.4 X 34.6 2.3 Am for l'hoesti monkeys, and 47.1 3.7 X 34.4 2.6 jm for vervets. Prevalence of infection with S. fulleborni did not differ between redtail guenons (7%) and blue monkeys (6%) (P > 0.05, Table 2-1).

Oxyuroidea: Eggs that appear to be Enterobius sp. based on egg size and

morphology were found in 2 redtail guenon samples (Table 2-1), and measured 64-66 X 36-37 jm (n = 2). This parasite is more reliably diagnosed by examination of peri-anal








skin or by necropsy (Ashford et al. 2000). Consequently, these prevalence values may be underestimations of actual prevalence.

Spiruroidea: Eggs that most closely resemble Streptopharagus sp. (symmetrical, larvated, thick-shelled) were found in feces of all guenon species, except l'hoesti monkeys, and measured 38.5 2.1 X 24.3 + 1.1 gm for redtail guenons, 40.1 + 1.9 X 25.0 1.3 pm for blue monkeys, and 41.7 1.8 X 25.6 1.5 jm for vervets. Prevalence of Streptopharagus sp. did not differ (P > 0.05) between redtail guenons (18%) and blue monkeys (14%) (P > 0.05, Table 2-1).

Cestoda

Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed oncosphere) were found in feces of only 1 redtail guenon, and measured 40-43 X 48-51 gm (n = 4); and no proglottids were detected through macroscopic inspection of feces (Table 2-1). Since eggs of this species are passed in proglottids, they are not mixed heterogeneously in feces. Consequently, these prevalence values may be gross underestimations of actual prevalence.

Trematoda

A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,

operculated, golden-brown coloration). Eggs were found in feces of all guenon species except l'hoesti monkeys, and measured 45.8 1.1 X 24.2 + 1.0 im for redtail guenons, 44 X 24 gm for blue monkeys, and 46 X 24 gm for vervets. Prevalence of this trematode did not differ (P > 0.05) between redtail guenons (2%) and blue monkeys (3%) (Table 21).








Protozoa

Cysts of 3 amoebae and 2 flagellates were identified from 235 fecal samples from redtail guenons. Cysts most closely resembling Entamoeba coli were multinucleate, with a mean diameter of 17.8 1.1 gm. Cysts most closely resembling Entamoeba histolytica had a mean diameter of 12.9 2.1. Cysts most closely resembling lodameoba butschlii had a single nucleus, distinct glycogen vacuole, and a mean diameter of 11.2 2.1. Cysts most closely resembling Giardia lamblia were ovoid with a mean diameter of 11.4 + 1.4. Cysts most closely resembling Chilomastix mesnili were lemon-shaped, with a mean diameter of 7.5 1.1. Prevalence in redtail guenons was relatively low for all protozoans; Entamoeba coli (11%), Entamoeba histolytica (10%), lodameoba butschlii (10%), Giardia lamblia (4%), and Chilomastix mesnili (1%). Effect of Season and Host Sex on Infection Prevalence

While prevalence did not correlate with monthly rainfall for any parasite species infecting redtail guenons (P > 0.496), seasonal fluctuations did occur (Figure 2-1). Although prevalence did not differ between male (n = 12) and female (n = 98) redtail guenons for any shared parasite species (P > 0.05), Oesophagostomum sp. (n = 24) and S. fulleborni (n = 16) infections were only detected in adult females. Variation in Prevalence among Sites throughout Africa

Previous studies have investigated the gastrointestinal parasites of blue monkeys from South Africa (Appleton et al. 1994) and Kenya (Munene et al. 1998). Comparisons with my study demonstrate great similarity in helminth faunas of blue monkeys among sites. However, prevalence varied greatly among sites. Trichuris sp. prevalence was lower in blue monkeys in Uganda compared to those in Kenya and South Africa (X2 = 11.96, P < 0.005). Prevalence of Oesophagostomum sp. in blue monkeys was higher in








Kenya than in Uganda, and higher in Uganda than in South Africa (X2 = 64.03, P <

0.001). Strongyloides sp. prevalence was higher in blue monkeys in Kenya compared to those in Uganda and South Africa (X2 = 93.85, P < 0.001). Prevalence of Streptopharagus sp. in blue monkeys was higher in South Africa than in Kenya, and prevalence in Kenya was higher than in Uganda (X2 = 54.66, P < 0.001). Infections of an anoplocephalid, thought to be Bertiella sp., were documented for blue monkeys in South Africa and Uganda and prevalence was higher in blue monkeys in South Africa compared to those in Uganda (X2 = 32.35, P < 0.001).

McGrew et al. (1989) reported on the gastrointestinal parasites of vervet monkeys in Senegal. Although Trichuris sp. infections were not documented, and another spiruroid nematode, Physaloptera sp., replaced Streptopharagus sp.; the overall helminth fauna was similar to that of vervets in my study.

Discussion

To my knowledge, this is the first report of gastrointestinal helminth parasites from wild populations ofredtail guenons and l'hoesti monkeys, and the first report of gastrointestinal helminth parasites from blue and vervet monkeys from Uganda.

The similarities in gastrointestinal parasite faunas among the guenons of western Uganda suggest that generalist parasites predominate, supporting the contention that in communities comprised of closely related species (i.e., Cercopithecus spp.), cross-species interaction may be an important source of infection risk (Ezenwa 2003). This may be one reason why redtail guenons associate with unrelated red colobus monkeys far more than with other guenon species (Chapman and Chapman 2000).

Seasonal patterns of infection were not readily apparent for any of the parasite species infecting redtail guenons. This result is unexpected, as previous studies of








primate parasite infections from tropical forest sites have documented an increase in prevalence during the rainy season (Freeland 1977; Huffmian et al. 1997). It is difficult to ascertain why seasonal differences were not seen in this study. However, fluctuation in infection prevalence was high, warranting future investigation of the mechanism behind these differences (Figure 2-1).

Although no differences in prevalence of infection were apparent between male and female guenons for shared parasite species, only adult females were infected with Oesophagostomum sp. and S. fulleborni. This may reflect energy and nutrient stress associated with producing and raising infants, which may result in an increased susceptibility to infection (Gulland 1992; Milton 1996).

Studies investigating the gastrointestinal parasites of blue monkeys, revealed

similar helminth faunas among sites (Appleton et al. 1994; Munene et al. 1998). This might be expected because of the recent origin of blue monkeys (Leakey 1988; Ruvolo 1988). However, parasite prevalence varied greatly among sites. In general, helminth prevalence was highest for Kenyan blue monkeys (with the exception of Streptopharagus sp., which had the highest prevalence for South African blue monkeys). In most cases, intermediate prevalence was seen in Ugandan compared to Kenyan and South African blue monkeys. Kenyan forests are small and fragmented, compared to those sampled in Uganda and South Africa (Appleton et al. 1994); and evidence presented in later chapters of this dissertation suggests that primates living in forest fragments may be more susceptible to infection, and demonstrate higher prevalence compared to conspecifics inhabiting large, undisturbed forests. This may explain the high prevalence of infection in Kenyan blue monkeys compared to the other 2 sites.








The helminth fauna of vervets was similar between Uganda and Senegal (McGrew et al. 1989). However, small sample size precluded comparisons of prevalence.

Freeland (1977) reported on the protozoan parasites of several primate species in Kibale National Park. His study identified 2 protozoans from redtail guenons not found in our study (i.e., Entamoeba hartmanni and an unidentified flagellate). Although Freeland (1977) does identify Chilomastix mesnili cysts from several species, they were not identified from redtail guenons. Despite these differences, the overall protozoan fauna of redtail guenons reported by Freeland (1977) and my study were similar. Unfortunately, Freeland (1977) does not provide data on prevalence.

My study contributes baseline data on the patterns of parasitic infection in wild guenons, providing a first step toward an index of population health and disease risk assessment for conservation and management plans of threatened guenon populations. My study also reveals that many of the gastrointestinal parasites of the guenon species examined may be zoonotic. Accordingly, future studies are needed to determine risks of cross-transmission. Mechanisms to reduce such risks would promote human health, livestock production, and local support for conservation.

Gastrointestinal parasite classification by fecal analyses is weak by its very nature. However it is the only responsible method to approach threatened species. Future studies employing molecular analyses and opportunistic necropsies are needed to improve our classification of the gastrointestinal parasites of guenons, and to improve our understanding of the risks of epizootic and zoonotic transmission.









Table 2-1. Prevalence (%) of gastrointestinal helminth parasite infections in guenons of western Uganda Parastie Species Redtail (n = 235) Blue (n = 35) L'hoiste (n = 11) Vervet (n = 12) Strongyloidesfulleborni 7 6 27 42 Oesophagostomum sp. 10 9 9 0 Unidentified Strongyle 0 0 0 42 Trichuris sp. 29 26 36 58 Streptopharagus sp. 18 14 0 17 Enterobius sp. 1 0 0 0 Bertiella sp. < 1 0 0 0 Dicrocoeliidae sp. 2 3 0 8 Overall 49 37 55 92



































Month


Figure 2-1. Inter-monthly variation in parasite infection prevalence of redtail guenons and rainfall at Kibale National Park, Uganda













CHAPTER 3
GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF UGANDA Introduction

Colobinae is a large subfamily of leaf-eating, old-world monkeys represented in Africa by two genera, Colobus and Piliocolobus (Grubb et al. 2002). These folivorous monkeys live in groups of highly variable size (5-300 individuals) and often form mixedspecies associations with other primates (Struhsaker 1981; Oates 1994; Chapman and Chapman 2000). Colobus species are forest-dependent, and consequently, acutely threatened by human activities that reduce forest cover. More than two-thirds of SubSaharan Africa's original forest cover has been lost due to anthropogenic disturbance (World Resources Institute 1998), and forest cover continues to decline at a rate of 0.7% annually (FAO 1999). Due largely to this habitat loss, 50% of African colobine species are endangered and an additional 20% are rare (Grubb et al. 2002).

Although parasite infections are common in nature and low-intensity infections are often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic change may result in a loss of stability associated with altered transmission rates, host range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline data on patterns of parasitic infections in wild colobine populations are critical to provide an index of population health and to begin to assess and manage disease risks.

Although many studies have documented the gastrointestinal parasites of wild populations of African apes (Huffmnan et al. 1997; Nizeyi et al. 1999; Graczyk et al., 1999; Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et








al. 1989; Mtiller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other African primate taxa remain poorly known. This study identifies and quantifies the prevalence of gastrointestinal helminth and protozoan parasites for the three colobus species of Uganda: the endangered red colobus (Piliocolobus tephroceles), the eastern black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus (Colobus angolensis). Where data are sufficient, I also examine the effect of season and host sex on parasite prevalence.

Materials and Methods

From August 1997 to July 2003, I collected 2,103 fecal samples: 1,608 from red colobus, 476 from eastern black-and-white colobus, and 19 from Angolan black-andwhite colobus. Red colobus and eastern black-and-white colobus samples were collected in 21 forest fragments in Western Uganda, and at Kanyawara, a 1,034 ha area characterized by logged and unlogged forest within Kibale National Park (766 kmn2; 0013'-0041' N, 30019'-30032' E; Struhsaker 1997). Mean annual rainfall (1990-2001) is 1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged 14.90C and 20.20C, respectively, from 1990 to 2001. Angolan black-and-white colobus samples were collected from three forest fragments adjacent to Lake Nabugabo in Southeastern Uganda (0020'-0025' S, 31 050'-31056' E). Annual rainfall ranges from 520 to 1,970 mm (Efitre et al. 2001) and daily temperature minima and maxima average 15.2oC and 27.2oC, respectively (Meteorology Department, Masaka, Uganda). All sites experience a bimodal pattern of seasonal rainfall, with peaks occurring in March-May and August-November (Figure 3-1).

Samples were collected immediately after defecation to avoid contamination and examined macroscopically for adult nematodes and tapeworm proglottids. Samples were








stored individually in 5.0-mL sterile vials in 10% formalin solution. Preserved samples were transported to the University of Florida where they were examined for helminth eggs and larvae and protozoan cysts using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Parasites were identified on the basis of egg or cyst color, shape, contents, and size. Iodine was used to facilitate protozoan identification. Measurements were made to the nearest 0.1 micron + SD using an ocular micrometer fitted to a compound microscope, and representatives were photographed. Coprocultures and necropsies (MAFF 1979) were used to match parasite eggs to larvae or adults for positive identification.

I performed chi-square tests of independence to compare the prevalence of

infections between colobus species and between host age and sex classes for a subset of red colobus (n = 401). Pearson correlation was used to test relationships between monthly rainfall and prevalence of parasites infecting red colobus and black-and-white colobus.

Results

Nematoda

Superfamily Trichuroidea: Trichuris sp. was identified based on egg size and

morphology (barrel-shape, yellow-brown coloration, and bipolar plugs) and verified by adults obtained by necropsy. Eggs were found in feces of all colobus species, and measured 57.3 1.0 X 27.0 1.3 gim for red colobus, 58.2 1.6 X 26.9 1.2 gm for eastern black-and-white colobus, and 58.8 1.2 X 27.2 1.4 gtm for Angolan black-andwhite colobus. Prevalence of T. trichiura was higher in Angolan black-and-white colobus than eastern black-and-white colobus (X2 = 5.28, d.f. = 1, P < 0.025, Table 3-1), and red colobus (X2 = 32.95, d.f. = 1, P < 0.001, Table 3-1). Prevalence T. trichiura was








higher in eastern black-and-white colobus than red colobus (X2 = 249.94, d.f. = 1, P <

0.001, Table 3-1).

Superfamily Strongyloidea: Oesophagostomum sp. was identified on the basis of egg size and morphology (elliptical and unlarvated) and verified by cultured larvae and adults obtained by necropsy. Eggs were found in feces of all colobus species except Angolan black-and-white colobus, and measured 70.0 1.4 X 41.8 1.6 ftm for red colobus and 70.2 1.8 X 41.6 1.6 gm for eastern black-and-white colobus. Prevalence of Oesophagostomum sp. was higher in eastern black-and-white colobus than in red colobus (X2 = 11.40, d.f. = 1, P < 0.001, Table 3-1).

Unidentified strongyle eggs were found in feces of all colobus species and

measured 59.6 5.6 X 38.2 4.1 gim for red colobus, 63.7 4.8 X 40.1 4.5 gm for eastern black-and-white colobus, and 68.4 2.0 X 40.3 2.3 jm for Angolan black-andwhite colobus. These strongyles may represent Necator sp., Ancylostoma sp., and/or Oesophagostomum sp.; however coprocultures were not performed, limiting our ability to identify these parasites to genus level. Prevalence of unidentified strongyles was higher for Angolan black-and-white colobus than for either red colobus (X2 = 9.18, d.f. = 1, P < 0.005, Table 3-1) or eastern black-and-white (X2 = 11.87, d.f. = 1, P < 0.001, Table 3-1).

Superfamily Rhabditoidea: Strongyloidesfulleborni was identified based on egg size and morphology (oval, thin-shelled, colorless, and larvated) and verified by cultured rhabditiform larvae. Eggs were found in feces of all colobus species, and measured 45.7 1.7 X 34.8 2.0 gm for red colobus, 46.7 2.2 X 35.2 2.2 ftm for eastern black-andwhite colobus, and 47.0 1.8 X 35.4 2.0 gm for Angolan black-and-white colobus. Prevalence of S. fulleborni did not differ among colobus species (P > 0.1, Table 3-1).








Strongyloides stercoralis was identified based on larvae size and morphology (rhabditiform esophagus, prominent genital primordium, and short buccal cavity). Strongyloides stercoralis larvae were found only in the feces of red colobus, and measured 242.4 4.5 gm in length.

Superfamily Ascaroidea: Ascaris sp. was identified based on egg size and

morphology (round or oval, thick-shelled, brown or yellow brown, and mammillated albuminous covering). Eggs were found in feces of red colobus and eastern black-andwhite colobus, and measured 65.2 + 1.3 X 55.8 + 1.1 gm and 63.9 + 1.4 X 54.4 + 1.0 gm, respectively. Prevalence of Ascaris sp. was higher for eastern black-and-white colobus

2
than for red colobus (X = 10.71, d.f. = 1, P < 0.005, Table 3-1).

Superfamily Oxyuroidea: Colobenterobius sp. was identified based on egg size and morphology (elliptical and thick-shelled) from red colobus and eastern black-andwhite colobus and and verified by adults obtained by necropsy. Colobenterobius sp. eggs were found in the feces of red colobus and eastern black-and-white colobus, and measured 64.8 1.6 X 36.4 1.4 jim and 65.3 + 1.2 X 36.6 + 1.6 gm, respectively. Prevalence of Colobenterobius sp. did not differ between colobus species (P > 0.1, Table 3-1). This parasite is more reliably diagnosed by examination of peri-anal skin or by necropsy (Ashford et al. 2000). Consequently, these prevalence values are likely an underestimation of prevalence.

Cestoda

Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed oncosphere) were found in feces of red colobus and eastern black-and-white colobus, and measured 40.3 + 0.8 X 48.8 + 1.2 pm and 41.2 + 1.4 X 50.0 1.0 pm respectively. No proglottids were detected through macroscopic inspection of feces. Prevalence of








Bertiella sp. did not differ between colobus species (P > 0.1, Table 3-1). Since eggs of this species are passed in proglottids, they are not mixed heterogeneously in feces. Consequently, these prevalence values are likely an underestimation of prevalence. Trematoda

A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,

operculated, golden-brown coloration). Eggs were found in feces of red colobus (46 X 24 jtm) and eastern black-and-white colobus (43.8 1.1 X 23.6 1.4 gm). Prevalence of Dicrocoelium sp. was higher for eastern black-and-white colobus than red colobus (X2

5.34, d.f. = 1, P < 0.025, Table 3-1).

Protozoa

Multinucleate cysts most closely resembling Entamoeba coli were found in the feces of all colobus species and had a mean diameter of 18.1 1.0 gm for red colobus, 17.4 1.4 pm for eastern black-and-white colobus, and 17.6 1.3 gm for Angolan blackand-white colobus. Prevalence of E. coli was higher for eastern black-and-white colobus than red colobus (X2 = 4.28, d.f. = 1, P <0.05, Table 3-1).

Cysts most closely resembling Entamoeba histolytica were found in the feces of all colobine species and had a mean diameter of 13.2 1.1 gm for red colobus, 12.5 1.8 gm for eastern black-and-white colobus, and 12.7 1.6 gm for Angolan black-and-white colobus. Prevalence of E. histolytica was higher for eastern black-and-white colobus than red colobus (X2 = 14.68, d.f. = 1, P < 0.001, Table 3-1).

Ovoid cysts most closely resembling Giardia lamblia were only found in the feces of red colobus and had a mean diameter of 11.9 1.8 jm (Table 3-1).








Effect of Season and Host Sex on Infection Prevalence

While prevalence did not correlate significantly with monthly rainfall for any

parasite species infecting red colobus (P > 0.077) or eastern black-and-white colobus (P > 0.081), variation over the year was evident (Figure 3-1).

Prevalence ofS. fulleborni was higher in adult male red colobus compared to adult females (X2 = 6.19, d.f. = 2, P < 0.05). However, prevalence did not differ for any other shared parasite species between age and sex classes (P > 0.05).

Discussion

To my knowledge, this is the first report of gastrointestinal parasites from wild populations of colobus monkeys. The similarities in gastrointestinal parasite faunas among the colobus of Uganda demonstrate that generalist parasites predominate. This supports the suggestion that in communities comprised of closely related species, crossspecies interaction may be an important source of infection risk (Ezenwa 2003). This may be one reason that colobines associate with unrelated guenons far more than with other colobus species (Chapman and Chapman 2000). It is also important to note that many of the species infecting colobines in Uganda occur at high frequency in the human populations in the region (NEMA 1997). Consequently, zoonotic and/or anthropozoonotic transmission may occur and may be promoted by various forms of anthropogenic disturbance.

Despite the great correspondence in parasite faunas among colobines, prevalence varied greatly with red colobus having the lowest prevalence and Angolan black-andwhite colobus having the highest prevalence. Prevalence is likely affected by complex interactions among environmental, demographic, genetic, and behavioral factors, making it difficult to explain this variation in prevalence. However, one relationship is








noteworthy. Unlike red colobus, eastern black-and-white colobus are known to descend into swampy areas to feed on aquatic vegetation (Oates 1978) where incidental ingestion of intermediate host or encysted trematodes is likely. Also, eastern black-and-white colobus are known to come to the group to eat soil and charcoal, much more frequently than red colobus (Gillespie pers. obs.). This may explain the higher prevalence of the dicrocoeliid liver fluke in eastern black-and-white colobus than red colobus.

Seasonal patterns of infection were not readily apparent for any of the parasite species infecting red colobus or eastern black-and-white colobus. This result is unexpected, as previous studies of parasite infections from tropical forest frugivorous monkeys and apes have documented an increase in prevalence during the rainy season (Lophocebus albigena Freeland 1977; Pan troglodytes Huffman et al. 1997). It is difficult to determine why seasonal differences were not seen in these folivores. However, variation in infection prevalence was evident over the year, warranting future investigation of the mechanism behind these differences (Figure 3-1).

Prevalence of S. fulleborni was higher in adult male compared to adult female red colobus. Perhaps this reflects energy and nutrient stress associated with maintaining social dominance (Hausfater and Watson 1976), which may result in an increased susceptibility to infection (Gulland 1992; Milton 1996). However, if this is the case, it is not clear why infection prevalence is not higher for other parasite species in males compared to females.

Freeland (1977) provided a survey of the protozoan parasites of primate species in Kibale National Park that failed to document the presence of any protozoan in colobus feces based on examination of a small number of samples for red colobus (n = 5) and








eastern black-and-white colobus (n = 7). This differs from my results, which demonstrate that colobines are susceptible to protozoan infection. However, my results reveal that protozoan prevalence for colobines is low compared to other primate species examined by Freeland (1977) (e.g., chimpanzees, baboons). Accordingly, it is likely that greater sampling effort during this earlier study would have yielded findings similar to my own.

This study contributes baseline data on the patterns of parasitic infection in wild

colobus monkeys, providing a first step toward an index of population health and disease risk assessment for conservation and management plans of threatened and endangered colobus populations. I documented that the vast majority of gastrointestinal parasites of wild colobus may be zoonotic or anthropozoonotic. Accordingly, future studies are needed to determine risks of cross-transmission. Mechanisms to reduce such risks may promote human health, livestock production, and local support for conservation.

Gastrointestinal parasite classification by fecal analyses is weak by its very nature. However it is the only responsible method to approach threatened species. Future studies employing molecular analyses and opportunistic necropsies are needed to improve our classification of the gastrointestinal parasites of guenons, as well as to improve our understanding of the risks of epizootic and zoonotic transmission.









Table 3-1. Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys of Uganda Parasite Species Piliocolobus tephroceles (n = 1.608) Colobus guereza (n = 476) Colobus angolensis (n =19)
Strongyloidesfulleborni 4 4 5 Strongyloides stercoralis < 1 0 0 Oesophagostomum sp. 3 6 0 Unidentified strongyle 2 1 11 Ascaris sp. < 1 1 0 Trichuris trichiura 38 79 1 Colobenterobius sp. < 1 1 0 Bertiella sp. < 1 < 1 0 Dicrocoelium sp. < 1 1 0 Entamoeba coli 4 8 16 Entamoeba histolytica 3 8 11 Giardia lamblia 1 0 0 Overall 38 79 100









A.


B., rcuiss.I--


Figure 3-1. Inter-monthly variation in parasite infection prevalence of colobus monkeys
and rainfall at Kibale National Park, Uganda. A) Red colobus monkeys. B)
Eatern Black-and-white colobus monkeys. (Grey bars represent rainfall.
Black lines represent parasite prevalence).













CHAPTER 4
LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN AFRICAN PRIMATE POPULATIONS

Introduction

With few areas legally protected from human exploitation, the conservation of

many species will depend on the capacity of disturbed areas to support their populations. Knowledge of how particular species are affected by specific forms of anthropogenic environmental change is essential for developing sound conservation and management plans, as well as assessing the relative conservation value of various disturbed habitats. Selective logging is a dominant habitat disturbance pattern with strong conservation potential (Frumhoff 1995; Struhsaker 1997; FAO 1999; Chapman and Peres 2001). A multitude of studies have examined the effects of selective logging on the abundance and diversity of invertebrate (Willott et al. 2000; Lewis 2001; Summerville and Crist 2002; Hamer et al. 2003) and vertebrate taxa (Johns and Skorupa 1987; Johns 1992; Heydon and Bulloh 1997; Marsden 1998; Robinson and Robinson 1999). Although logging often results in a reduction in overall diversity, effects on individual species are difficult to predict. The nature and intensity of response appear to vary depending on species and site characteristics. For example, following heavy logging at Kibale National Park in Uganda, red colobus monkeys (Piliocolobus tephroceles) declined, while black-andwhite colobus monkeys (Colobus guereza) increased in density (Chapman et al. 2000). Another primate, the blue monkey (Cercopithecus mitis) declined after logging at Kibale,








but increased following similar intensity logging at another site in Uganda (Plumptre and Reynolds 1994; Chapman et al. 2000).

Ninety percent of primate species are restricted to the tropics, and the majority are forest dependent (Chapman and Peres 2001). Consequently, with 5 to 6 million ha of tropical forest selectively logged each year (FAO 1990; FAO 1999), it is not surprising that primates have been the focus of much research concerning the impact of logging on biodiversity (Johns and Skorupa 1987; Johns 1997; Struhsaker 1997; Chapman et al. 2000). Although logging is known to negatively impact the abundance of some primate species, the proximate mechanism for these declines remains unknown. Implied mechanisms include altered ranging patterns (Johns 1997) and reduced food-tree density (Skorupa 1988; Struhsaker 1997; Chapman et al. 2000). However, contrasting sites to arrive at generalities is often difficult, as some areas experience increased hunting pressure after logging, while others areas do not (Mittermeier 1987; Peres 1990; Oates 1994; Robinson and Bennett 2000). Support for the operation of particular mechanisms for primate declines following logging is largely indirect and it is unlikely that a single correlate will explain the complex relationship between primate declines and logginginduced ecological change. The potential role of parasites and infectious disease in such primate population declines remains largely unexplored.

Helminthic and protozoal parasites can impact host survival and reproduction

directly through pathological effects and indirectly by reducing host condition (Chandra and Newberne 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous abortion, congenital malformations, and death (Chandra and Newberne 1977;








Despommier et al. 1995). However, less severe infections are more common and may impair nutrition, travel, feeding, predator escape, and competition for resources or mates; or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate mechanisms, parasites can potentially regulate host populations (Gregory and Hudson 2000; Hochachka and Dhondt 2000).

Selective logging results in changes in forest structure and food availability

(Skorupa 1988; Ganzhorn 1995; Chapman and Chapman 1997; Chapman et al. 2000). Such changes may alter parasite dynamics in wildlife populations. For example, Ganzhom (1995) demonstrated that selectively logged forests have higher foliage density than unlogged forests. Higher foliage density translates to greater surface area exposed to falling feces and possibly an increased probability of contact with infected fecal material for arboreal animals. In addition, many forest species are stressed following selective logging due to reduced food availability. Various forms of environmental stress have been suggested to increase susceptibility to parasitic infection, and stress and disease are thought to act synergistically to increase morbidity and mortality (Scott 1988; Holmes 1996; Lafferty and Holt 2003). Reductions in animal condition due to food stress have been documented to increase vulnerability to infection, and result in lower fertility and higher mortality (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). In addition, animal body condition and reproductive status are compromised when parasites inflict substantial energetic costs (Hudson 1986; Moller 1993; Toque 1993; Rigby and Moret 2000). However, parasites do not necessarily induce negative effects if hosts have a sufficient energy or nutrient surplus concurrent with infection (Munger and Karasov








1989; Gulland 1992; Milton 1996). This suggests that the outcome of host-parasite associations may be contingent on host nutritional status as well as severity of infection.

Emerging infectious diseases have raised global awareness of the potential impact ecological change can have on biodiversity conservation and wildlife and human health (Meffe 1999; Daszak et al. 2000; Patz et al. 2000; Deem et al. 2001; Lafferty and Gerber 2002). To better develop strategies to deal with established and changing patterns of disease, we must understand the interplay among alteration and fragmentation of ecosystems, wildlife-human disease linkages, and the ecology of novel diseases. This study aims to improve our understanding of this interplay by examining the effects of selective logging on parasite dynamics in three primate species, the redtail guenon (Cercopithecus ascanius), the red colobus (Piliocolobus tephroceles), and the black-andwhite colobus (Colobus guereza) in Kibale National Park, Uganda. I compare the prevalence, diversity, and mean number of gastrointestinal parasite species infecting individuals, and the relative infection risk between primates from logged and undisturbed forests. My investigation proposes explanations for similarities and differences in parasite dynamics between logged and undisturbed forests and addresses the implications of these findings to conservation and management strategies.

Materials and Methods

Study Site

Kibale National Park (766 km2) is located in western Uganda (lat 0013'-0041' N, long 30019'-30o32' E) near the base of the Ruwenzori Mountains (Struhsaker 1997). Tall, closed-canopy forest accounts for 57% of the park. The remainder forms a mosaic of swamp (4%), grasslands (15%), pine plantations (1%), and colonizing forest (19%) (Chapman and Lambert 2000). The study site, Kanyawara, is located at the northern end








of the park at an elevation of 1,500 m (Gillespie and Chapman 2001). Kanyawara experiences a bimodal pattern of seasonal rainfall, with peaks occurring in March-May and August-November. Mean annual rainfall (1990-2001) is 1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged 14.90C and 20.20C, respectively, from 1990 to 2001.

Prior to becoming a National Park in 1993, Kibale was a Forest Reserve, gazetted in 1932 with the stated goal of providing a sustained production of hardwood timber (Osmaston 1959). A polycyclic felling cycle of 70 years was initiated, and it was recommended that logging open the canopy by approximately 50% through the harvest of trees> 1.52 m in girth (Kingston 1967). This history of logging has led to varying degrees of disturbance among sites. I conducted my study in two forestry compartments; one logged at high intensity in the late 1960s (K-15), and one undisturbed (K-30).

The K-15 forestry compartment is a 347-ha section of forest that experienced highintensity, selective felling from September 1968 through April 1969. Total harvest averaged 21 m3/ha or approximately 7.4 stems/ha (Struhsaker 1997), but incidental damage was much higher. It is estimated that approximately 50% of all trees in compartment K-15 were destroyed by logging and incidental damage (Skorupa 1988). A total of 18 tree species were harvested, with nine species contributing more than 95% of the harvest volume (Kasenene 1987; Skorupa 1988). Many of the tree species harvested provided primates with food (Struhsaker 1997; Chapman et al. 2000).

The K-30 forestry compartment is a 282-ha area that has not been commercially harvested. Prior to 1970, however, a few large stems (0.03-0.04 trees/ha) were removed by pitsawyers. This extremely low level of extraction seems to have had little effect on








the structure and composition of the forest (Skorupa and Kasenene 1984; Struhsaker 1997). Hence, compartment K-30 serves as a control plot for my comparisons. As a control, I assume that differences between the undisturbed compartment and the logged compartment are due only to the effects of logging. This is not ideal as some differences could be the result of naturally occurring variation in forest structure. However, these compartments are in close proximity (< 2 km apart), and there are few marked differences between them in terms of physical characters that influence forest structure.

The study area has been protected from human exploitation since the 1970s, and the hunting of primates ceased in the region in the early 1960s (Struhsaker 1997; Chapman et al. 2000). The site's primates have been studied extensively, with over 30 years of primate research and substantial background information on the majority of primate species present (Struhsaker 1997; Chapman et al. in press). For these reasons, a number of primate groups are habituated, encounter rate is high, and long-term data are available on several groups for most primate species. Fecal Sampling and Analysis

From August 1997 to August 2002, I collected 1,076 fecal samples from primates in forest compartments K-15 and K-30; 157 from red-tail guenons, 231 from black-andwhite colobus, and 688 from red colobus. All samples were collected immediately after defecation to avoid contamination and examined macroscopically for adult nematodes and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile vials in a 10% neutral formalin solution. Preserved samples were transported to the University of Florida where they were examined for helminth eggs and larvae and protozoan cysts using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994; Greiner and Courtney 1999). Parasites were counted and identified on the basis of egg or








cyst color, shape, contents, and size. Iodine was occasionally used to facilitate protozoan identification. Measurements were made to the nearest 0.1 micron + SD using an ocular micrometer fitted to a Zeiss compound microscope. Unknown parasites were photographed for later identification. Coprocultures and necropsies were used to match parasite eggs to larvae and adult worms for positive identification (MAFF 1979; Greiner and Courtney 1999). I report data on helminth eggs per gram of feces (EPG) only as an indication of environmental contamination (i.e., infection risk), as helminth egg production is highly variable and rarely indicative of actual infection intensity. Infection Risk Assessment

From January to August 2002, I conducted a comparative survey to determine an index of risk of helminth infection to primates inhabiting logged and undisturbed forests. Canopy vegetation, ground vegetation, and soil plots from logged and unlogged forests were collected and analyzed to determine the density of infective-stage individuals for the two parasite species most prevalent in all three primate species, Trichuris sp. (eggs) and Oespohagostomum sp. (L3 larvae). Twenty-eight 1 m3 vegetation plots were collected at a height of 12 m from canopy trees used within the previous two hours by red colobus; 14 from logged forest (K-15), and 14 from undisturbed forest (K-30). Access to the canopy for collection of vegetative plots was facilitated by single rope climbing technique (Mitchell, 1982; Laman, 1995). An additional 28 1 m3 ground vegetation plots were collected below all trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches) were collected within selected ground vegetation plots, 10 from the logged forest and 10 from the unlogged forest. I used a modified sedimentation technique to recover infectivestage parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using a modified Baermann method (Sloss et al. 1994). Samples from all plots were examined








by dissecting and compound scope. Infective-stage primate parasites were identified and counted.

Statistical Analyses

I employed chi-square tests of independence to compare the prevalence of infection between the logged and undisturbed forests for overall and specific infections for each of the three primate species. Independent sample t-tests were performed to compare the mean number of parasite species infecting individual primates and the density of infective-form parasites in vegetative plots between the logged and undisturbed forests (SPSS, version 10, 1999).

Results

Infection Prevalence and Richness

Descriptions of taxa, mode of infection, and associated pathology for each parasite species recovered can be found in Table 4-1. The prevalence of infection with Trichuris sp., Streptopharagus sp., Strongyloidesfulleborni, Oespohagostomum sp., Entamoeba coli, E. histolytica, and lodameoba buetschlii was higher for redtail guenons from logged forest compared to guenons from undisturbed forest (Table 4-2). Only redtail guenons from logged forest were infected with Enterobius sp., a dicrocoeliid liver fluke, Bertiella sp., Giardia lamblia, and Chilomastix mesnili (Table 4-2). There were no species of parasite found only in undisturbed forest. The mean number of parasite species infecting individual redtail guenons was greater in logged compared to undisturbed forest (t = 5.74, P < 0.001, Figure 4-1).

The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum sp., E. coli, and E. histolytica did not differ between red colobus from logged and undisturbed forest (Table 4-3). Only red colobus from undisturbed forest were infected








with Colobenterobius sp. (Table 4-3). The mean number of parasite species infecting individual red colobus did not differ between logged and undisturbed forest (t = 1.32, P

0.186, Figure 4-1).

The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum sp., the dicrocoeliid liver fluke, E. coli, and E. histolytica did not differ between blackand-white colobus from logged and undisturbed forest (Table 4-4). Only black-and-white colobus from logged forest were infected with Colobenterobius sp. and Bertiella sp. (Table 4-4). The mean number of parasite species infecting individual black-and-white colobus did not differ between logged and undisturbed forest (t = 0.64, P = 0.524, Figure 4-1).

Infection Risk

Trichuris sp. eggs were more abundant in canopy plots (Disturbed Mean = 1.43 + 0.20, Undisturbed Mean = 0.47 0.25, t = -2.66, P = 0.013) and ground vegetation plots (Disturbed Mean = 4.21 + 0.13, Undisturbed Mean = 0.43 + 0.96 t = -3.56, P = 0.003) from logged compared to undisturbed forest. Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots from logged compared to undisturbed forest (Disturbed mean = 3.93 + 1.23, Undisturbed mean = 0.14 0.11, t= -3.14, P = 0.008), but were not found in canopy plots. No infective-stage primate parasites were identified from the soil plots.

Discussion

A recent study demonstrated that group densities for redtail and blue guenons at Kibale were lower in logged forest than undisturbed forest and that their populations declined between censuses conducted 12 and 28 years after logging (Chapman et al. 2000). Although Chapman et al. (2000) found red colobus densities to be lower in








logged forest than undisturbed forest, their populations were in a state of recovery. In contrast, the study found black-and-white colobus densities to be higher in logged forest than in undisturbed forests.

The current study provides insights into the variable responses to logging observed in these redtail guenon, red colobus, and black-and-white colobus populations. It is clear that logging at Kibale has altered parasite dynamics resulting in higher densities of infective-stage parasites common to both guenons and colobines. Despite this higher infection risk for all three primate species, only redtail guenons manifest higher prevalence and richness of gastrointestinal parasite infections and a higher mean number of parasite species infecting individuals in logged compared to undisturbed forests. These results suggest that guenons are more susceptible to parasitic infection following selective logging than colobines.

The greater long-term impact of logging on guenon compared to colobine

populations may be a function of altered parasite dynamics in association with food availability and animal nutrition and condition. Dietary stress may adversely affect resistance to parasitic infection by reducing the effectiveness of the immune system (Crompton 1991, Solomons and Scott 1994, Holmes, 1995, Milton 1996). As a result, food shortages could result in higher parasite intensity, which in turn could increase nutritional demands on the host and accentuate the effects of food shortages. Under such conditions, nutritional status and parasitism could have synergistic effects on the host and the individual effects of each factor would be amplified when co-occurring (Mihook et al. 1985, Keymer and Dobson 1987, Holmes 1995).








There is good evidence that logging has greatly reduced guenon food availability at Kibale. First, recall that approximately 50% of all trees in logged forests were destroyed by felling and incidental damage and that trees harvested were disproportionately primate food trees (Skorupa 1988; Struhsaker 1997). This reduction in food availability following logging likely accounts for much of the initial declines seen in guenon and red colobus populations. Second, even 25 years after logging, tree growth rates and tree density for all size classes were lower, while seedling mortality was higher in the logged compared to undisturbed forests (Chapman and Chapman 1997). This suggests that logged forests are regenerating poorly. So why have red colobus started to recover, while guenons have not in logged forests? Recall that selective logging facilitates higher foliage density as a result of greater sunlight availability (Ganzhorn 1995). This translates to greater food availability and food quality (e.g., a predominance of young leaves) for the folivorous colobines. In addition, the tree species that colonize disturbed areas (i.e., Celtis durandii and Funtumia latifolia) have leaves with a higher protein-tofiber ratio (i.e., higher food quality; Milton 1998), a component of leaves important in determining colobine abundance (Chapman and Chapman 2002). From 1990 to 2000, the total basal area of both C. durandii and F. latifolia, major food species for both colobines, increased substantially in the logged forest (Chapman and Chapman, in press). During this same period, growth rates for both of these tree species were higher in the logged compared to the undisturbed forests (Chapman and Chapman, in press). Concurrently, food resources for the frugivorous guenons have not been recovering. Multiple indices of fruit production demonstrated lower fruit availability in the logged compared to undisturbed forests even 25 years after logging (Chapman and Chapman








1997). In addition, at both 22 and 32 years post-logging, the basal area of trees in logged forests was less than in undisturbed forests (Chapman and Chapman, in press). Thus, a primary guenon food resource, mature fruit-bearing trees, were reduced significantly in density by logging and young trees are not successfully regenerating to replace those lost to logging. Consequently, it is not surprising that red colobus have begun to recover in parallel with their food resources; while guenons have not recovered.

Although food availability accounts well for the lack of recovery in guenon

populations in logged forests, it is not clear why populations are declining. However, nutrition and parasite dynamics may interact to play a role in these declines. Correlations among elevated parasitism, reduced nutrition, and reduced body condition are well documented (Mori 1979, Eley et al. 1989; Gulland 1992; Milton 1996); however, causation remains equivocal. Milton (1996) demonstrated that howler monkey (Alouatta palliata) mortality was best explained by the interaction of age, physical condition, dietary stress, and intensity of parasitic bot fly infestations. Similarly, Gulland (1992) found that the timing of population crashes in Soay sheep (Ovis aries) were strongly correlated with emaciation, high intensity nematode infections, and signs of proteinenergy malnutrition. Moreover, free-ranging sheep treated with antihelminthics had lower mortality rates, while experimentally infected sheep fed nutritious diets showed no sign of malnutrition. Recent evidence from Kibale indicates that dietary stress affects redtail guenons in logged forests. These guenons have lower intake of crude protein and the majority of key minerals compared to guenons in undisturbed forests (K. Rode, personal communication). Such protein deficiencies have been linked to depressed immune function (Chandra 1983; Bundy and Golden 1987; Koski and Scott 2001). In








addition, nutrient content varies more among food items for guenons compared to colobines at Kibale (K. Rode, personal communication). Thus, variation in nutritional condition is likely more sensitive to changes in habitat for guenons than for colobines.

Parasite infections are common in nature and low-intensity infections are often

asymptomatic. Endemic stability is common, resulting in coexistence of parasite, vector (in vector-borne parasites), host, and environment such that clinical disease is rare (Norval et al 1992). However, anthropogenic change may result in a loss of endemic stability associated with altered vector dynamics, transmission rates, parasite host range, and parasite virulence (Deem et al. 2001). Resultant high-intensity infections, as well as moderate-intensity infections in stressed animals, can result in morbidity and mortality.

Comparisons of parasite prevalence can be a useful indirect indicator that parasites may be impacting host populations (i.e., population declines correlated to increased infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting guenons at higher prevalence in the logged forests have the capacity to cause substantial pathology and death in primates (Table 4-1). Heavy infections of Oesophogostomum sp., Strongyloides sp., and Enterobius sp. are associated with mucosal inflammation, ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and Johnsen 1978; Holmes et al. 1980; Harper et al. 1982; Liu et al. 1995; Murata et al. 2002). Even moderate intensities of Oesophogostomum sp. have proven clinically important in stressed captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For example, nearly 30% of 70 guenons imported to Italy from Senegal died soon after arrival from severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent








complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of all parasites infecting guenons in logged forests at Kibale may contribute to greater morbidity and mortality in this guenon population compared to the population inhabiting undisturbed forests.

The magnitude and prevalence of multiple-species infections in individuals can be another useful indirect indicator that parasites may be impacting host populations. Multiple-species infections are associated with a greater potential for morbidity and mortality due to synergistic and competitive interactions occurring between parasite species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sebelis 1995). For example, concurrent infections with Heligmosomoides polygurus and Trypanosoma congolense in mice (Fakae et al. 1994) and Escherichia coli and Ascaris suum in pigs (Adedeji et al. 1989) result in higher mortality than single infections. Similarly, in humans, Schistosoma. mansoni has an increased effect on the development of malnutrition in the presence of T. trichiura (Parraga et al. 1996) and a range of parasites demonstrate greatly elevated pathogenic effects in the presence of HIV (Gomez et al. 1995; Kaplan et al. 1996). Consequently, the elevated frequency and number of multiplespecies infections observed in guenons in logged forests at Kibale may contribute to greater morbidity and mortality in this guenon population compared to the population inhabiting undisturbed forests.

Other dietary differences between guenon and colobine species may also play a role in the patterns observed. Encounter probabilities for some of the parasites involved would be expected to differ between guenons and colobines. Bertiella sp., Dicrocoelium sp. and Streptopharagus sp. have intermediate hosts. Guenons feed on many of these








intermediate hosts, which include coleopterans, orthopterans, ants, and land snails, while colobines do not intentionally feed on insects and other invertebrates. Consequently, if intermediate hosts are more common in logged forests or more intermediate hosts are infected in logged forests, guenons may have a higher encounter probability for parasites with indirect life cycles. However, infections with these parasite species are rarely associated with disease, thus, they are likely of minor importance in regards to guenon declines in logged forests (Table 4-1).

This study suggests that redtail guenons are more susceptible to parasitic infection than colobines following selective logging at Kibale National Park in Uganda. Logging in Kibale is known to impact these frugivorous guenon populations more than folivorous colobine populations, and parasite dynamics appear to play a role in these patterns of response. Consequently, conservation initiatives for guenons, and potentially a widerange of frugivorous species, should focus on the preservation of intact forests. However, extractive management plans that avoid the removal of preferred food species, maintain arboreal pathways, and reduce infection risk may allow for selective logging without the loss of frugivorous populations.

Although many recent studies and reviews have focused on the conservation

implications of anthropozoonotic disease transmission to wildlife (Stuart and Strier 1995; Wallis and Lee 1999; Nizeyi et al. 2001; Graczyk et al. 2002; Woodford et al. 2002), the potential impact of anthropogenic habitat disturbance on disease dynamics in wild populations has received far less attention. This study demonstrates that one such disturbance, selective logging, has the capacity to alter parasite dynamics for some species. Knowledge of how particular species are affected by various forms of ecological








change is essential to promote land-use policy that is compatible with animal and human health and biodiversity conservation.

Our understanding of how anthropogenic habitat change alters wildlife disease

dynamics is in its infancy. Our comprehension of this interplay will be greatly improved by future research that investigate how selective logging and other forms of anthropogenic habitat disturbance affect the rates and patterns of parasite and disease transmission within and between species. In addition, studies are needed that explore how nutritional state modulates the effects of parasites and the occurrence of disease in wild populations. Identifying risk factors for disease transmission will improve the ability of conservationists to make rational decisions about the risks and benefits of extraction and management activities.









Table 4-1. Mode of infection, morbidity, and mortality associated with gastrointestinal parasites infecting redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda
Parasite Species Mode of Infection Morbidity/Mortality Sources Trichuris sp. Embryonated egg ingested Typically asymptomatic Beaver et al. 1984; Baskin 1993

Streptopharagus sp. Intermediate host ingested Typically asymptomatic Beaver et al. 1984; Coombs and (cockroach, beetle) Crompton 1991 Strongyloidesfulleborni Larvae ingested, skin Mucosal inflammation, McClure and Guilloud 1971; penetration ulceration, death Pampiglione and Ricciardi 1972 Oesophagostomum sp. Larvae ingested Severe diarrhea, weight loss, Crestian and Crespeau 1975; death Roperto et al. 1985
Enterobius sp. Egg ingested Dysentary, enteritis, ulceration, Liu et al. 1995; Murata et al. 2002 death
Colobenterobius sp. Egg ingested Dysentary, enteritis, ulceration, Hugot 1999 death
Dicrocoeliid liver fluke Metacercaria ingested in ant Typically asymptomatic Beaver et al. 1984; Coombs and or on vegetation Crompton 1991 Bertiella sp. Cysticercoid ingested in Typically asymptomatic Fiennes 1967; Lloyd 1998 orbatid mite
Giardia lamblia Cyst or trophozoite ingested Typically asymptomatic, Fiennes 1967; Baskin 1993 possibly epizoonotic
Entamoeba coli Cyst or trophozoite ingested Typically asymptomatic Beaver et al. 1984

Entamoeba histolytica Cyst or trophozoite ingested Hepatic and gastric amoebiasis, Loomis 1983 death
Chilomastix mesnili Cyst or trophozoite ingested Typically asymptomatic Beaver et al. 1984

lodameoba buetschlii Cyst or trophozoite ingested Typically asymptomatic Beaver et al. 1984










Table 4-2. Prevalence (%) of gastrointestinal parasite infections in redtail guenons (Cercopithecus ascanius) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species Logged (n = 235) Undisturbed (n = 35) Significance Trichuris sp. 63 21 *** Streptopharagus sp. 32 13 Strongyloidesfulleborni 16 4 **


Oesophagostomum sp. Enterobius sp. Dicrocoeliid liver fluke Bertiella sp. Giardia lamblia Entamoeba coli Entamoeba histolytica Chilomastix mesnili Iodameoba buetschlii

Overall


N.A.

N.A.

N.A.

N.A.


N.A.
***


* P < 0.05, ** P < 0.01, *** P < 0.001, N.A. no chi-square test performed since one forest type had 0 prevalence









Table 4-3. Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus tephroceles) from logged and undisturbed
forests in Kibale National Park, Uganda
Parasite Species Logged (n = 127) Undisturbed (n = 561) Significance Trichuris sp. 40 36 N.S. Strongyloidesfulleborni 1 4 N.S. Oesophagostomum sp. 5 2 N.S. Colobenterobius sp. 0 1 N.A. Entamoeba coli 6 3 N.S. Entamoeba histolytica 6 3 N.S. Overall 45 37 N.S. N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence









Table 4-4. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species Logged (n = 125) Undisturbed (n = 106) Significance Trichuris sp. 79 84 N.S. Strongyloidesfulleborni 4 3 N.S. Oesophagostomum sp. 9 9 N.S. Colobenterobius sp. 2 0 N.A. Dicrocoeliid liver fluke 1 1 N.S. Bertiella sp. 1 0 N.A. Entamoeba coli 16 9 N.S Entamoeba histolytica 16 9 N.S. Overall 79 84 N.S.


N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence











SUndisturbed U Logged


Redtail Guenon


Red Colobus


Black-and-White Colobus


Figure 4-1. Mean number of parasite species infecting individual redtail guenon (Cercopithecus ascanius), red colobus (Piliocolobus
tephroceles), and black-and-white colobus (Colobus guereza) in undisturbed and logged forest at Kibale National Park,
Uganda













CHAPTER 5
ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES IN FOREST FRAGMENTS

Introduction

Forest fragmentation reduces overall species diversity and alters species abundance (Laurance and Bierregaard 1997; Laurance 1999); modifying biological processes such as predation, competition, and infection dynamics (Crooks and Soule 1999; Terborgh et al. 2001; LoGuidice et al. 2003). To date, empirical evidence has been lacking to test the relative importance of these factors in explaining the complex relationship between wildlife declines and fragmentation-induced ecological change. I present support for a previously unrecognized mechanism for vertebrate declines following forest fragmentation, altered infection dynamics.

Parasite infections are common in nature and low-intensity infections are often

asymptomatic. Stability is common, resulting in coexistence of parasite, vector, and host such that clinical disease is unusual (Anderson and May 1979; May and Anderson 1979). However, anthropogenic change may result in a loss of stability associated with altered vector dynamics, transmission rates, parasite host range, and parasite virulence (May 1988; Daszak et al. 2000; Patz et al. 2000). Resultant changes in host susceptibility and infection risk may result in elevated morbidity and mortality, and ultimately, population declines.

Forest fragmentation results in a suite of alterations that may increase susceptibility to infection and infection risk in resident populations (Figure 5-1). Environmental








stressors associated with forest fragmentation, such as reduced food availability and diversity, density-dependent factors, and more frequent interactions with humans may reduce immunity and elevate susceptibility to infection (Murray et al. 1998; Lafferty and Holt 2003). Reduced habitat area following forest fragmentation may result in restricted ranging and crowding (McCallum and Dobson 2002; Lafferty and Holt 2003), increasing habitat overlap among conspecifics, thus predisposing individuals to a higher probability of pathogen contact (Freeland 1977; Altizer 2003). Landscape characteristics of fragment boundaries influence the frequency and nature of contact among wildlife, human, and livestock populations, increasing the potential for epizootic and anthropozoonotic pathogen transmission (Lafferty and Gerber 2002; McCallum and Dobson 2002).

To improve our understanding of how fragmentation alters infection dynamics, I quantified gastrointestinal parasites of the endangered red colobus (Piliocolobus tephroceles) and black-and-white colobus (Colobus guereza) populations in western Uganda between August 1999 and July 2003. I compare the prevalence, diversity, number of gastrointestinal parasite species infecting individuals, and relative infection risk for primates between forest fragments and undisturbed forests within Kibale National Park. Concurrent censuses of colobus populations allowed us to examine infection dynamics in relation to host-population dynamics. Our investigation proposes a novel mechanism for vertebrate declines in forest fragments and addresses implications of these findings for conservation strategies.








Materials and Methods

Study Site

I surveyed 20 forest fragments that lie within the agricultural landscape from the

western boundary of Kibale National Park to the foothills of the Ruwenzori Mountains in Uganda (0o13'-0041' N, 30019'-30032') (Onderdonk and Chapman 2000). Mean annual rainfall in the region is 1749 mm (1990-2001) and mean daily minimum and maximum temperatures are 14.90C and 20.20C, respectively (1990-2001, Chapman and Chapman unpublished data). Rainfall is bimodal, with two rainy seasons generally occurring from March to May and September to November.

Prior to agricultural expansion, mid-elevation, moist, evergreen forest dominated the region (Naughton-Treves 1997). While the precise timing of isolation of these forest remnants is not known, local elders describe them as 'ancestral forests', and aerial photographs from 1959 confirm that most have been isolated from Kibale since at least that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha, are used by local citizens to varying degrees, and are surrounded by small-scale agriculture or tea plantations.

I surveyed compartment K-30, a 282-ha area of undisturbed forest situated within the largely forested Kibale National Park (746 km2)(Struhsaker 1997). Compartment K30 is in close proximity to the forest fragments (< 6.5 km apart), and once belonged to the same tract of forest, minimizing the probability that differences observed are the result of inherent variation in forest structure and diversity. Fecal Sampling and Analysis

From August 1999 to July 2003, I collected 1,151 fecal samples from primates in 20 forest fragments and the K-30 compartment of Kibale National Park: 951 from red








colobus and 200 from black-and-white colobus. All samples were collected immediately after defecation to avoid contamination and examined macroscopically for adult nematodes and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile vials in a 10% formalin solution. Preserved samples were transported to the University of Florida where they were examined for helminth eggs and larvae and protozoan cysts using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Parasites were counted and identified on the basis of egg or cyst color, shape, contents, and size. Iodine was occasionally used to facilitate protozoan identification. Measurements were made to the nearest 0.1 micron + SD using an ocular micrometer fitted to a compound microscope. Unknown parasites were photographed for later identification. Coprocultures and necropsies were used to match parasite eggs to larvae and adult worms for positive identification (MAFF 1979). Infection Risk Assessment

As an index of infection risk, infective-stage parasite densities were determined for canopy vegetation, ground vegetation, and soil plots from fragmented and undisturbed forest. From January to August 2002, I collected twenty-nine 1 m vegetation plots at a height of 12 m from canopy trees used within the previous 2 hr by red colobus; 15 from forest fragments and 14 from undisturbed forest. Canopy access for plot collection was facilitated by single rope climbing technique (Mitchell 1982). An additional 29 1 m3 ground vegetation plots were collected below all trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches) were collected within randomly selected ground vegetation plots, 10 from forest fragments and 10 from undisturbed forest. I used a modified sedimentation technique to recover infective-stage parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using a modified Baermann method








(Sloss et al. 1994). Samples were examined by dissecting and compound scope, and infective-stage individuals of the two most prevalent parasite species, Trichuris trichuria (eggs) and Oespohagostomum stephanostomum (L3 larvae) were counted. Colobus Surveys

Red colobus and black-and-white colobus populations in forest fragments were censused from May to August 2000 and recensused May to August 2003. The total number of colobus in each fragment was counted over 1 to 4 days. Our repeated censuses of red colobus and black-and-white colobus over the past three decades within the K-30 compartment of Kibale National Park provide comparable data for these colobus populations (Chapman et al. 2000). Statistical Analyses

I employed chi-square tests of independence to compare prevalence between

fragment and undisturbed forest samples for overall and specific infections. Independent sample t-tests were performed to compare mean number of parasite species infecting individual primates and density of infective-form parasites in plots between fragmented and undisturbed forest.

Results

Infection Prevalence and Richness

The prevalence of infection with Trichuris sp., Oespohagostomum sp., Entamoeba coli, and Entamoeba histolytica was higher for red colobus from forest fragments compared to red colobus from undisturbed forest, but prevalence did not differ for Strongyloidesfulleborni or Colobenterobius sp. (Table 5-1). Only red colobus from forest fragments were infected with Strongyloides stercoralis, Ascaris sp., Bertiella sp., Giardia lamblia, and unknown strongyles (Table 5-1). There were no species of parasite








found only in undisturbed forest. The number of parasite species infecting individual red colobus was greater in forest fragments compared to undisturbed forest (t = -5.785, P <

0.001, Figure 5-2).

For black-and-white colobus, the prevalence of infection with Trichuris sp., S.

fulleborni, Oespohagostomum sp., a dicrocoeliid liver fluke, E. coli, and E. histolytica did not differ between animals in forest fragments and undisturbed forest (Table 5-2). Only black-and-white colobus from forest fragments were infected with Ascaris sp. and unknown strongyles (Table 5-2). There were no species of parasite found only in undisturbed forest. The number of parasite species infecting individual black-and-white colobus did not differ between forest fragments and undisturbed forest (t = -0.219, P=

0.827, Figure 5-2).

Infection Risk

Trichuris sp. eggs were more abundant in canopy plots (fragmented mean = 1.36

0.35 eggs/plot, undisturbed mean = 0.47 0.25 eggs/plot, t = -2.43, P = 0.022) and ground vegetation plots (fragmented mean = 1.87 0.48 eggs/plot, undisturbed mean =

0.43 + 0.26 eggs/plot, t = -2.40, P = 0.026) from fragmented compared to undisturbed forest. Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots from fragmented compared to undisturbed forest (fragmented mean = 3.33 + 0.64 larvae/plot, undisturbed mean = 0.14 0.11 larvae/plot, t= -4.95, P < 0.001), but were not found in canopy plots. No infective-stage primate parasites were identified from the soil plots.

Colobus Population Dynamics

Ten of the 20 forest fragments censused contained red colobus and persisted for the duration of the study (i.e., were not cleared). In these fragments, red colobus declined








from 163 individuals in 2000 to 131 individuals in 2003, a 20% reduction. Twelve of the forest fragments censused contained black-and-white colobus and persisted for the duration of the study. In these fragments, black-and-white colobus increased from 97 individuals in 2000 to 101 individuals in 2003, a 4% increase. Results of red colobus and black-and-white colobus censuses over the past three decades in the K-30 compartment of Kibale National Park demonstrate that densities of both colobus species are stable (Chapman et al 2000).

Discussion

My results demonstrate that forest fragmentation has altered infection dynamics resulting in higher densities of infective-stage parasites common to red colobus and black-and-white colobus. Despite this higher infection risk for both species, only red colobus manifested higher prevalence and richness of gastrointestinal parasite infections and a higher number of parasite species infecting individuals in fragmented compared to undisturbed forests. These results suggest that red colobus are more susceptible to parasitic infection following forest fragmentation than black-and-white colobus.

Reduced food availability and diversity is likely the critical environmental stressor responsible for this elevated susceptibility of red colobus to infection following forest fragmentation. Compared to intact forest, fragments have been documented to have higher rates of tree mortality (Mesquita et al. 1999), increased densities of trees with wind- or water dispersed seeds, and reduced densities of trees with vertebrate-dispersed seeds (Tabarelli et al. 1999), of which smaller fruited species predominate (Chapman and Onderdonk 1998). These trends predict an overall reduction in food resources for frugivorous and folivorous vertebrates in forest fragments. For species sensitive to changes in food availability, resultant food stress may increase susceptibility to infection.








This appears to be the case for the red colobus. Red colobus typically consume a high diversity diet (i.e., > 42 species) and their density can be predicted from the abundance of important food trees (Struhsaker 1975; Chapman et al. 2002). Such broad dietary requirements might predispose red colobus to food stress in forest fragments, where the necessary diversity of plant species and parts are not always available (Chapman et al. 2003b). In contrast, black-and-white colobus have a low diversity diet (i.e., < 25 species with 3 species accounting for 69%) and demonstrate a high degree of dietary flexibility (Onderdonk and Chapman 2000; Oates 1974). They are clearly capable of persisting on a monotonous diet dominated by readily available tree species, an advantage for living in forest fragments with high variation in tree species composition (Chapman et al. 2003b). However, one population of red colobus has been documented to persist on a very monotonous diet (Chapman et al. 2002) and as fragments are degraded red colobus are often the last species to remain. Correlating stress hormones with variation in food availability and quality would provide insights into whether or not this factor is responsible for this elevated susceptibility of red colobus to infection following forest fragmentation.

Comparisons of parasite prevalence can be a useful indirect indicator that parasites may be impacting host populations (i.e., population declines correlated to increased infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting red colobus at higher prevalence in forest fragments have the capacity to cause substantial pathology and death in primates (Table 3). High intensity infections of Oesophogostomum sp. and Strongyloides sp. are associated with mucosal inflammation, ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and








Johnsen 1978). Even moderate intensities of Oesophogostomum sp. have proven clinically important in stressed captive primates (Crestian and Crespeau 1975; Soulsby 1982). For example, nearly 30% of 70 guenons imported to Italy from Senegal died soon after arrival from severe oesophogostomiasis (Roperto et al 1985). Secondary bacterial infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of parasites infecting red colobus in forest fragments may contribute to greater morbidity and mortality in this colobus population compared to the population inhabiting undisturbed forests.

The magnitude and prevalence of multiple-species infections in individuals can be another useful indirect indicator that parasites may be impacting host populations. Multiple-species infections are associated with a greater potential for morbidity and mortality due to synergistic and competitive interactions occurring between parasite species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sabelis 1995). Consequently, the elevated frequency and number of multiple-species infections observed in red colobus in forest fragments may contribute to greater morbidity and mortality in this colobus population compared to the population inhabiting undisturbed forests.

My results demonstrate that humans, and potentially livestock, are exposing colobus in forest fragments to novel pathogens. Four species infecting red colobus (Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified strongyle) and two species infecting black-and-white colobus (Ascaris sp. and an unidentified strongyle) are likely anthropozoonotic or epizootic in origin. These parasites occur at high frequency in the human populations in the region (NEMA 1997), but are absent








from colobus within Kibale National Park, where the people and primates interact at a reduced frequency. In addition, the majority of colobine parasites appear to be generalists and occur in the local human population (NEMA 1997). These are the pathogens of greatest concern for rare species, such as the red colobus (Lafferty and Gerber 2002). Humans and livestock may act as reservoirs, maintaining a high infection risk for parasites that are detrimental to red colobus, even as red colobus densities decline toward extinction (McCallum and Dobson 2002). Likewise, considering the extensive overlap in parasite communities between the colobine species, black-and-white colobus may also be acting as reservoirs for most red colobus parasites. Consequently, it will be important to recognize the importance of generalist parasites within a community context to preserve sensitive species, such as the endangered red colobus.

Our understanding of how anthropogenic habitat change alters wildlife disease

dynamics is in its infancy. Our comprehension of this interplay will be greatly improved by future research that investigates how forest fragmentation and other forms of anthropogenic habitat disturbance affect the rates and patterns of parasite transmission within and among species. In addition, studies are needed that explore if and how nutritional state modulates the effects of parasites and the occurrence of disease in wild populations. Identifying risk factors for disease transmission will improve the ability of conservationists to make rational decisions about the risks and benefits of extraction and management activities.









Table 5-1. Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus tephroceles) from forest fragments and
undisturbed forests in Kibale National Park, Uganda
Parasite Species Fragmented (n = 390) Undisturbed (n = 561) Significance Trichuris sp. 50 36 *** Unidentified strongyle 6 0 N.A. Strongyloidesfulleborni 5 4 N.S. Strongyloides stercoralis 2 0 N.A. Oesophagostomum sp. 4 2 Ascaris sp. < 1 0 N.A. Colobenterobius sp. < 1 1 N.S. Bertiella sp. < 1 0 N.A. Entamoeba coli 13 3 *** Entamoeba histolytica 10 3 ** Giardia lamblia 6 0 N.A. Overall 50 37 ***

* p < 0.05, ** p < 0.005, *** p < 0.001, N.S. p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence.









Table 5-2. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from forest fragments
and undisturbed forests in Kibale National Park, Uganda
Parasite Species Fragmented (n -= 94) Undisturbed (n = 106) Significance Trichuris sp. 90 84 N.S. Unidentified strongyle 5 0 N.A. Strongyloidesfulleborni 7 3 N.S. Oesophagostomum sp. 4 9 N.S. Ascaris sp. 6 0 N.A. Entamoeba coli 6 9 N.S. Entamoeba histolytica 5 9 N.S. Overall 90 84 N.S. N.S. p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence










Forest Fragmentation


Reduced Tree Density 8 Diversity


Reduced Habitat Area


Increased Contact with Humans 6 Livestock
I


Reduced Food Availability Restricted Ranging Crowding Chronic Stress Introduction of Novel Pathogens Reduced Immunity 8 Elevated Susceptibility to Infection Elevated Infection Risk


Population Declines


Figure 5-1. Conceptual model of proposed mechanism for population declines in forest











Undisturbed U Fragmented


d0


0 I


Red Colobus


Black-and-White Colobus


Figure 5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus tephrosceles), and black-and-white colobus
(Colobus guereza) in undisturbed and fragmented forest Western Uganda.













CHAPTER 6
VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST FRAGMENT ATTRIBUTES

Introduction

For fragmented forests to have conservation value, they must retain ecological integrity sufficiently to maintain species and biological processes over the long-term. Studies have highlighted the importance of physical attributes such as fragment size, shape, and isolation (Laurance and Bierregaard 1997); and biological attributes such as predator, prey, and tree density and diversity on ecological processes and species survival probabilities (Crooks and Soule 1999; Terborgh et al. 2001; Laurance et al. 2002). However, despite the large scope of this research, our capacity to predict how ecological processes will be altered and which taxonomic or functional groups will be most affected by fragmentation is still poor.

Such difficulties are well illustrated by primates inhabiting forest fragments. No clear generalizations emerge as to what types of primates are most susceptible to fragmentation, nor what types of fragments are most likely to support primates, despite a growing body of research (Tutin et al. 1997; Onderdonk and Chapman 2000; Marsh 2003). Our inability to evaluate the potential of forest fragments for primate conservation appears to be driven by several factors. First, most previous work has been conducted in fragments protected from human use (Lovejoy et al. 1996; Tutin et al. 1997; Gilbert 2003); however, typically fragments are not protected and are characterized by open access by private citizens who depend on them for fuelwood, medicinals, or bushmeat








(Chapman et al. 2003). While studies involving protected fragments have provided us with many insights, they may have biased our perception of the value of forest fragments for conservation.

Second, a number of simple logical predictions relating to primates in forest

fragments have not proven to be general. For example, home range size was frequently cited as influencing a species ability to survive in a fragment (Lovejoy et al 1986; Estrada and Coates-Estrada 1996). However, Onderdonk and Chapman (2000) found no relationship between home range size and ability to live in fragments for a community of primates in western Uganda. Similarly, it has been suggested that a highly frugivorous diet may limit the ability of a species to live in fragments (Lovejoy et al 1986; Estrada and Coates-Estrada 1996). However, Tutin et al. (1997) found that several frugivorous species were at higher or similar densities in forest fragments than in the intact forest of Lop6 Reserve, Gabon (see also Tutin 1999; Onderdonk and Chapman 2000).

Lastly, past studies have often focused on simple correlates to primate population viability in forest fragments. However, finding such single correlative explanations for complex biological phenomena, like determinants of primate abundance in fragments, is unlikely. Rather, recent long-term studies have highlighted the importance of multifactoral explanations. For example, based on a 68-month study of howler monkeys (Alouattapalliata) and a parasitic bot fly (Alouattamyia baeri), Milton (1996) concluded that the annual pattern of howler mortality results from a combination of effects including: age, physical condition, and larval burden of the parasitized individual, which becomes critical when the population experiences dietary stress (see also Milton et al. 1994). Similarly, Gulland (1992) studied the interactions of Soay sheep and nematode








parasites and demonstrated that at times of population crashes sheep were emaciated, had high nematode burdens, and showed signs of protein-energy malnutrition. In the field, sheep treated with antihelminthics had lower mortality rates, while experimentally infected sheep with high parasite loads, but fed nutritious diets, showed no sign of malnutrition. The potential role of parasites and infectious disease in primate population dynamics in forest fragments remains largely unexplored.

Helminthic and protozoal parasites can impact host survival and reproduction

directly through pathological effects and indirectly by reducing host condition (Chandra and Newberne 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous abortion, congenital malformations, and death (Chandra and Newberne 1977; Despommier et al. 1995). However, less severe infections are more common and may impair nutrition, travel, feeding, predator escape, and competition for resources or mates; or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate mechanisms, parasites can potentially regulate host populations (Gregory and Hudson 2000; Hochachka and Dhondt 2000).

To improve our capacity to evaluate the conservation value of forest fragments, I examined how various fragment attributes affect one ecological process, parasite infection dynamics, and consider how changes in this process may impact host populations of red colobus (Piliocolobus tephrosceles) inhabiting a series of forest fragments in western Uganda.








Materials and Methods

Study Site

Nine forest fragments that support red colobus that lie within the agricultural

landscape adjacent to the western boundary of Kibale National Park and in the foothills of the Ruwenzori Mountains in Uganda were surveyed. Mean annual rainfall in the region is 1749 mm (1990-2001) and mean daily minimum and maximum temperatures are 14.90C and 20.20C (1990-2001). Rainfall is bimodal, with two rainy seasons generally occurring from March to May and September to November.

Prior to agricultural expansion; mid-elevation, moist, evergreen forest dominated the region (Naughton-Treves 1997). While the precise timing of isolation of these forest remnants is not known, local elders describe them as 'ancestral forests', and aerial photographs from 1959 confirm that most have been isolated from Kibale since at least that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha and occur in areas largely unsuitable for agriculture (i.e., forested swampy valley bottoms, steep forested rims of crater lakes; Table 6-1). These fragments are used by local citizens to varying degrees and are surrounded by small-scale agriculture or tea plantations (Table 61).

Fecal Sampling and Analysis

From August 1999 to July 2003, I collected 536 fecal samples from red colobus in forest fragments to determine the prevalence of infection with strongyle and rhabditoid nematodes, a group of potentially pathogenic parasites. All samples were collected immediately after defecation to avoid contamination and examined macroscopically for adult nematodes. Samples were stored individually in 5.0 mL sterile vials in a 10% neutral formalin solution. Preserved samples were transported to the University of








Florida where they were examined for nematode eggs and larvae using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Nematodes were counted and identified on the basis of egg color, shape, contents, and size. Measurements were made to the nearest 0.1 micron + SD using an ocular micrometer fitted to a compound microscope. Coprocultures and necropsies (MAFF 1979) were used to match nematode eggs to larvae and adult worms for positive identification. Infection Risk Assessment

To obtain an index of infection risk, I determined infective-stage parasite densities for canopy vegetation, ground vegetation, and soil plots from fragments with high stump density (Kiko 3) and low stump density (Nkuruba). From January to August 2002, I collected thirty 1 m3 vegetation plots at a height of 12 m from canopy trees used within the previous two hours by red colobus; 15 from each fragment. Canopy access for plot collection was facilitated by single rope climbing technique (Mitchell, 1982; Laman, 1995, Houle et al. 2004). Thirty 1 m3 ground vegetation plots were collected below all trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches) were collected within randomly selected ground vegetation plots, 10 from forest fragments and 10 from undisturbed forest. I used a modified sedimentation technique to recover infective-stage parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using a modified Baermann method (Sloss et al. 1994). Samples were examined by dissecting and compound scope, and infective-stage individuals of the most prevalent strongyle nematode, Oespohagostomum sp. (L3 larvae) were counted. Fragment Characteristics

Forest fragment attributes quantified included fragment size, fragment type, distance to Kibale, distance to the nearest fragment, trees/ha, tree species/ha, tree








stumps/ha, red colobus/ha, and total colobines/ha. The size of each fragment was measured, taking GPS readings at locations along fragment edges and/or measuring fragment perimeters with a 50 m tape (Onderdonk and Chapman 2000). Fragments were classified as crater lake, hillside, or valley bottom. Crater lake and hillside fragments (n = 4) were forests on steep hills or sides of explosion craters; for analyses, they are considered together. Valley-bottom fragments (n = 5) have swamp vegetation associated with their lowest levels. Consequently, valley-bottom fragments may retain greater humidity, potentially providing a better environment for the development of strongyle nematodes during their free-living stage. Distance to Kibale National Park and nearest fragment are straight-line distances measured from topographic maps. At each fragment, all trees > 10 cm DBH (Diameter at Breast Height; Chapman et al. 2003) were identified and measured. Sizes of trees on very steep craters were visually estimated (error in visual estimation = + 3.7%, N = 46). As colobus rarely feed in small trees (Gillespie and Chapman 2001), this represents a nearly complete inventory of all colobus potential food sources. Tree stumps remaining after harvest by local people were also counted. This involved carefully searching through vine tangles and dense herbaceous vegetation in search of hidden stumps. For most tree species, the stump will remain for several years, providing an index of habitat degradation.

Since parasite dynamics could be influenced by host density, the density of red colobus and black-and-white colobus (Colobus guereza) were determined via observations made over 24-hours at each fragment. I include red colobus, as well as total colobus, density among biological attributes examined, since black-and-white colobus may serve as a reservoir host for red colobus infection with shared parasites.








Results

Mean fragment size for the 9 fragments surveyed was 5.11 ha and fragments ranged from 1.20 to 8.70 ha (Table 6-1). Five of the fragments were classified as valley bottom and 4 were crater lake or hillside (Table 6-1). Mean distance to Kibale National Park was 2.4 km and ranged from 0.2 to 6.5 km (Table 6-1). Mean distance to the nearest fragment was 142 m and ranged from 50 (the criteria for a isolated fragment) to 500 m (Table 6-1). Mean tree density was 133 trees/ha and ranged from 27 to 445 trees/ha (Table 6-1). Mean tree species/ha was 15.9 tree species/ha and ranged from 4 to 73 tree species/ha (Table 6-1). The level of degradation of the fragments was highly variable and stump density ranged from 0.16 to 221.76 stumps/ha and averaged 69.2 stumps/ha (Table 6-1). Stumps density reflects the intensity of extraction in these fragments, which was associated with beer brewing, gin distillation, and charcoal production by households bordering a fragment (Chapman et al 2003). Red colobus density averaged 3.70 red colobus/ha and ranged from 0.55 to 8.33 red colobus/ha (Table 6-1). Mean colobine density (red colobus and black-and-white colobus) was 5.52 colobines/ha and ranged from 1.66 to 9.41 colobines/ha (Table 6-1).

Two strongyle (Oespohagostomum sp. and an unidentified strongyle) and 2

rhabditoid nematodes (Strongyloidesfulleborni and S. stercoralis) were found from red colobus inhabiting forest fragments (Table 6-2). Mean prevalence among fragments of Oespohagostomum sp. was 5%, but prevalence ranged from 0 to 24 %. Mean prevalence of the unidentified strongyle was 8% and ranged from 0 to 28%. S. fulleborni prevalence averaged 6% among fragments and ranged from 0 to 16%. The prevalence of S. stercoralis was the lowest of all nematodes examined averaging 2% among fragments,








but it ranged from 0 to 12. Collectively, the prevalence of strongyles and rhabditoids was 20% and ranged from < 1% to 68%.

Individually and collectively, the prevalence of all strongyle and rhabditoid

nematodes was positively correlated with stump density (Table 6-3). With the exception of Oespohagostomum sp., prevalence of all strongyles and rhabditoids individually and collectively, was negatively correlated with fragment size (Table 6-3). Strongyloides stercoralis prevalence was positively correlated with red colobus and total colobine density (Table 6-3).

When predicting strongyle and rhabditoid prevalence using a step-wise multiple

regression that included stump density, fragment size, and colobus density; stump density entered the model first explaining 85% of the variance (F = 38.84, R2= 0.847, P < 0.001). Subsequently, no other variable entered the model suggesting that fragment degradation, indexed by stump density, was the most important variable in predicting strongyle and rhabditoid prevalence and once this variable was considered, there was little remaining variance that could be explained by other variables measured. Stump density was correlated with fragment size (r--0.811, P- 0.008), and colobus density (r=0.657, P=-0.054).

A similar situation was found when predicting Oespohagostomum sp. (F = 13.41, R2 = 0.608, P = 0.008), S. fulleborni (F = 21.64, R2 = 0.756, P = 0.002), S. stercoralis (F = 71.66, R2 = 0.911, P < 0.001), and the unidentified strongyle prevalence (F = 9.93, R2 =

0.587, P = 0.016), in that only stump density entered the model.

Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots from Kiko 3, the fragment with high stump density, compared to Nkuruba, which had








low stump density (Kiko 3 mean = 3.33 0.64 larvae/m3, Nkuruba mean = 0.82 + 0.98 larvae/m3, t= -2.87, P = 0.005). However, Oesophagostomum sp. L3 larvae were not found in canopy or soil plots.

Discussion

The results of this study demonstrate that an index of habitat degradation, stump

density, best explained the prevalence of strongyle and rhabditoid nematode infections in red colobus in forest fragments in western Uganda. I also found a greater risk of infection with Oesophagostomum sp., a representative strongyle, for red colobus in the fragment with the highest stump density compared to the fragment with the lowest stump density. In some cases, fragment size and colobine density were also related to strongyle and rhabditoid prevalence, but these variables did not explain a significant amount of variation that was independent of stump density.

These results may provide insights into observed declines in red colobus in the forest fragments of western Uganda. As noted earlier, red colobus declined in these forest fragments by 20% between surveys in 2000 and 2003. Altered parasite dynamics may play a role in these declines. Although parasite infections are common in nature and low-intensity infections are often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic change may result in altered transmission rates, parasite host range, and parasite virulence (Daszak et al. 2000; Patz et al. 2000). Resultant changes in host susceptibility may result in elevated morbidity and mortality, and ultimately, population declines.

The strongyle and rhabditoid nematodes documented to infect red colobus in this study have the capacity to cause substantial pathology and death in primates. Heavy infections of Oesophogostomum spp. and Strongyloides spp. have been associated with








mucosal inflammation, ulceration, dysentery, weight loss, and death in primates (McClure and Guilloud 1971; DePaoli and Johnsen 1978; Holmes et al. 1980; Harper et al. 1982). Even moderate intensities of Oesophagostomum sp. have proven important in stressed or captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For example, nearly 30% of 70 guenons imported to Italy from Senegal died soon after arrival from severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent complications of oesophogostomiasis (Soulsby 1982). Even more troubling are S. stercoralis and unidentified strongyle infections, which are likely anthropozoonotic in origin. These parasites occur at high frequency in the human populations in the region, but are absent from colobus within Kibale National Park, where the people and primates interact at a reduced frequency. Since S. stercoralis parasitic females live in the superficial tissues of the small intestine, and can be present in high numbers due to autoinfection, they can cause significant pathology in humans (Pappas and Wardrop 1999).

Considering the potential role that strongyle and rhabditoid nematode infections may play in red colobus declines in forest fragments, we should investigate ways to mitigate alterations in infection dynamics in the face of extraction.









Table 6-1. Physical and biological attributes of forest fragments with red colobus (Piliocolobus tephroceles) populations near Kibale
National Park, Uganda
Fragment Distance to Nearest
Fragment Size (ha) Type Kibale (km) Fragment (m) Trees/ha Tree species/ha Stumps/ha Red Colobus/ha Colobines/ha Bugembe 4.68 VB 2.5 500 52 8.76 71.18 2.35 2.35 CK 8.70 HS 0.2 150 41 4.94 45.75 2.87 3.68 Kifuruka 7.24 CL 6.5 95 27 4.03 12.42 0.55 1.66 Kiko 1 6.20 VB 2.0 50 42 6.61 56.45 3.55 4.19 Kiko 2 5.00 VB 1.8 125 63 4.00 8.40 2.80 5.20 Kiko 3 1.70 VB 1.1 70 231 12.94 221.76 4.71 9.41 Kiko 4 1.20 VB 1.1 70 259 20.83 174.17 8.33 8.33 Nkuruba 6.40 CL 3.6 70 445 73.00 0.16 3.44 6.72 Rutoma 4.90 HS 3.0 150 34 7.76 32.24 4.69 8.16 Average 5.11 N.A. 2.4 142 133 15.87 69.17 3.70 5.52











Table 6-2. Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus monkeys (Piliocolobus tephroceles) in
forest fragments near Kibale National Park, Uganda


Oesophagostomum sp.

3 2 2 5 7 24

3


Unidentified Strongyle Strongyloidesfulleborni

16 6 2 0


Strongyloides stercoralis Collective

0 25 0 4 0 6 9 34 0 16 12 68 0 17


Fragment Bugembe CK

Kifuruka Kiko 1I Kiko 2 Kiko 3 Kiko 4 Nkuruba Rutoma Average


N 31 66 53 45 40 25 44 179 53 N.A.










Table 6-3.Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus monkeys (Piliocolobus tephrosceles) and
attributes of the forest fragments they inhabit near Kibale National Park, Uganda

Oesophagostomum sp. Unidentified Strongyle Strongyloides fullebomrni Strongyloides stercoralis Collective


Fragment Size Fragment Type Distance to Kibale Nearest Fragment Trees / ha Tree sp. / ha Red Colobus / ha Colobines / ha Stumps / ha


-0.581 (p = 0.101)


-0.220 (p = 0.570)


-0.336 (p = 0.377)


-0.204 (p = 0.598) 0.201 (p = 0.605)


-0.128 (p = 0.744) 0.239 (p = 0.536) 0.459 (p = 0.214)


0.811 (p = 0.008)**


-0.730 (p = 0.025) *


-0.409 (p = 0.274)


-0.393 (p = 0.296) 0.285 (p = 0.458) 0.109 (p = 0.780)


-0.199 (p = 0.607) 0.010 (p = 0.980) 0.267 (p = 0.487)


0.766 (p = 0.016) **


-0.835 (p = 0.005) **


-0.014 (p = 0.971)


-0.401 (p = 0.285)


-0.291 (p = 0.448) 0.422 (p = 0.258) 0.012 (p = 0.976)


0.672 (p = 0.047) 0.691 (p = 0.039) *


0.954 (p < 0.001) **


-0.811 (p = 0.008) **


-0.185 (p = 0.634)


-0.417 (p = 0.264)


-0.019 (p = 0.962) 0.199 (p = 0.608)


-0.184 (p = 0.635) 0.437 (p = 0.240) 0.511 (p = 0.160)


0.920 (p < 0.001) **


(n = 9 for all comparisons, Pearson Correlation and corresponding P-value provided)


-0.777 (p = 0.014) **


0.049 (p = 0.901)


-0.328 (p = 0.389)


-0.121 (p = 0.757) 0.142 (p = 0.715)


-0.226 (p = 0.560) 0.442 (p = 0.234) 0.367 (p = 0.331)


0.869 (p = 0.002) **













CHAPTER 7
SUMMARY AND CONCLUSIONS

Emerging infectious diseases have raised global awareness of the potential impact

that ecological change can have on biodiversity conservation and wildlife and human

health. This study improves our understanding of this interplay by examining the effects

of logging and forest fragmentation on parasite dynamics in an African primate

community. The most important contributions of this study are as follows.

1. This study provided the first reports of gastrointestinal helminth parasites from wild
populations of redtail guenons, l'hoesti monkeys, red colobus, and black-and-white
colobus and the first report of gastrointestinal helminth parasites from blue and
vervet monkeys from Uganda. This baseline data on the patterns of parasitic
infection in wild monkeys provides a first step toward an index of population health
and disease risk assessment for conservation and management plans of threatened
and endangered African primate populations.

2. This study demonstrated that selective logging was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus, black-and-white colobus, and redtail guenons. Despite this higher infection risk for all species, only redtail guenons manifested higher
prevalence and richness of gastrointestinal parasite infections and greater
magnitude multiple-infections in logged compared to undisturbed forests. These
results suggest that redtail guenons are more susceptible to parasitic infection
following selective logging than colobines.

3. This study demonstrated that forest fragmentation was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus and black-and-white colobus. Despite this higher infection risk for both species, only red colobus manifested higher prevalence and richness of
gastrointestinal parasite infections and greater magnitude muliple-infections in
fragmented compared to undisturbed forests. These results suggest that red colobus
are more susceptible to parasitic infection following forest fragmentation than
black-and-white colobus.

4. This study demonstrated that humans, and potentially livestock, are exposing
colobus in forest fragments to novel pathogens. Four species infecting red colobus
(Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified





81


strongyle) and two species infecting black-and-white colobus (Ascaris sp. and an unidentified strongyle) are likely anthropozoonotic or epizootic in origin. These parasites occur at high frequency in the human populations in the region, but are absent from colobus within Kibale National Park, where the people and primates
interact at a reduced frequency.

5. This study demonstrated that an index of habitat degradation, stump density, best
explained the prevalence of strongyle and rhabditoid nematode infections in red
colobus in forest fragments in western Uganda. This coincided with a greater risk
of infection with Oesophagostomum sp.,a representative strongyle nematode, for
red colobus in the fragment with the highest stump density compared to the
fragment with the lowest stump density. Considering the potential role that these nematode infections may play in red colobus declines in forest fragments, future
studies should investigate ways to mitigate alterations in infection dynamics in the
face of extraction.














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Full Text
11
African primate taxa remain poorly known. The present study identifies and quantifies
the gastrointestinal helminth parasites for the 4 guenon species of western Uganda: redtail
guenons (Cercopithecus ascanius), blue monkeys (C. mitis), l'hoesti monkeys (C.
Ihoesti), and vervet monkeys (C. aethiops). For the most common species (the redtail
guenon), I also report protozoan parasites, and examine the effect of season and host sex
on parasite prevalence.
Materials and Methods
From January 1998 to December 2002,1 collected 293 fecal samples from free-
ranging guenons at forested sites in western Uganda; 235 from redtail guenons, 35 from
blue monkeys, 11 from l'hoesti monkeys, and 12 from vervet monkeys. Samples from
redtail guenons, blue monkeys, and lhoesti monkeys were collected in Kanyawara, a
1,034 ha area characterized by logged and unlogged forest within Kibale National Park
(766 km2; 013'-04r N, 3019'-3032' E; Struhsaker 1997). Samples from vervet
monkeys were collected at Lake Saka, a forest fragment 30 km northwest of the national
park. The region experiences a bimodal pattern of seasonal rainfall, with peaks occurring
in March-May and August-November (Figure 2-1). Mean annual rainfall (1990-2001) is
1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged
14.9C and 20.2C, respectively, from 1990 to 2001.
Samples were collected immediately after defecation to avoid contamination, and
were examined microscopically for adult nematodes and tapeworm proglottids. With the
exception of redtail guenons, samples represent individuals. In the case of redtail
guenons, samples are the result of repeated collections from approximately 150 animals.
Samples were stored individually in 5.0-mL sterile vials in 10% neutral formalin solution.
Preserved samples were transported to the University of Florida, where they were


87
Gilbert K.A. 1994. Endoparasitic infection in red howling monkeys (Alouatta seniculus)
in the Central Amazonian Basin: a cost of sociality? Ph.D. Dissertation, Rutgers
University, NJ.
Gilbert K.A. 2003. Primates and fragmentation of the Amazon forest. Pp. 145-158,
in L.K. Marsh, ed. Primates in Fragments: Ecology and Conservation. Kluwer
Academic/Plenum Publishers, New York.
Gillespie T.R. and C.A. Chapman. 2001. Determinants of group size in the red colobus
monkey (Procolobus badius): an evaluation of the generality of the ecological-
constraints model. Behavioral Ecology and Sociobiology. 50:329-338.
Gomez M.A., C. Atzori, A. Ludovisi, P. Rossi, M. Scaglia, and E. Pozio. 1995.
Opportunistic and non-opportunistic parasites in HIV-positive and negative patients
with diarrhoea in Tanzania. Tropical Medical Parasitology 46:109-114.
Graczyk T.K., J. Bosco-Nizeyi, B. Ssebide, R.C.A. Thompson, C. Read, M.R. Cranfield.
2002. Anthropozoonotic Giardia duodenalis genotype (assemblage) A infections in
habitats of free-ranging human-habituated gorillas, Uganda. Journal of Parasitology
88:905-909.
Graczyk T.K., L.J. Lowenstine, and M.R. Cranfield. 1999. Capillaria heptica
(Nematoda) infections in human-habituated mountain gorillas (Gorilla gorilla
beringei) of the Parc National de Volcans, Rwanda. Journal of Parasitology
85:1168-1170.
Gregory R.D. and P.J. Hudson. 2000. Population biology: parasites take control. Nature
406:33-34.
Greiner E. and C. Courtney. 1999. Veterinary Parasitology. College of Veterinary
Medicine, University of Florida, Gainesville, FL.
Grieser Johns A. and B. Grieser Johns. 1995. Tropical forest primates and logging: long
term coexistence? Oryx 29:205-211.
Grubb P., T.M. Butynski, J.F. Oates, S.K. Bearder, T.R. Disotell, C.P. Groves, and T.T.
Struhsaker. 2002. An Assessment of the Diversity of African Primates. IUCN/SSC
Primate Specialist Group, Washington, D.C.
Gulland F.M.D. 1992. The role of nematode parasites in Soay sheep (Ovis aries L.)
mortality during a population crash. Parasitology 105:493-503.
Hahn N.E., D. Proulx, P.M. Muruthi, S. Alberts, and J. Altmann. 2003. Gastrointestinal
parasites in free-ranging Kenyan baboons (Papio cynocephalus and P. anubis).
International Journal of Primatology 24:271-279.


12
examined for helminth eggs and larvae, and protozoan cysts, using concentration by
sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Parasites were
identified on the basis of egg or cyst color, shape, contents, and size. Iodine was used to
facilitate protozoan identification. Measurements were made to the nearest 0.1 p SD,
using an ocular micrometer fitted to a compound microscope; and representatives were
photographed. Mean egg sizes presented are based on measurement of 10 eggs from 10
different hosts unless otherwise noted. Coprocultures (10 per guenon species except
vervets), were used to match parasite eggs to larvae for positive identification of
strongylate nematodes (MAFF 1979). Our capacity to identify most parasite species
from host fecal examination, even with cultured larvae, is limited. Thus, I present most
of my findings at the level of family or genus.
I performed chi-square tests of independence to compare the prevalence of
infections between redtail guenons and blue monkeys. Small sample size precluded me
from including l'hoesti and vervet monkeys in these comparisons. Chi-square tests of
independence were also performed to compare prevalence between host sex for redtail
guenons, and to compare prevalence for the blue monkey population to previously
published reports. I used Pearson correlations to test for relationships between monthly
rainfall and prevalence of parasites infecting redtail guenons.
Results
Nematoda
Trichuroidea: Trichuris sp. was identified based on egg size and morphology
(barrel-shape, yellow-brown coloration, and bipolar plugs). Eggs were found in feces of
all guenon species, and measured 55.1 1.2 X 27.2 1.1 pm for redtail guenons, 60.0
2.0 X 27.0 1.4 pm for blue monkeys, 58.3 1.2 X 27.1 1.1 pm for l'hoesti monkeys,


84
Chapman C.A. and L.J. Chapman. 1999. Implications of small scale variation in
ecological conditions for the diet and density of red colobus monkeys. Primates
40:215-232.
Chapman C.A. and L.J. Chapman. 2000. Interdemic variation in mixed-species
association patterns: common diurnal primates of Kibale National Park, Uganda.
Behavioral Ecology and Sociobiology 47:129-139.
Chapman C.A. and L.J. Chapman. 2002. Foraging challenges of red colobus monkeys:
Influence of nutrients and secondary compounds. Comparative Biochemistry and
Physiology 133:861-875.
Chapman CA, L.J. Chapman, and T.R. Gillespie. 2002. Scale issues in the study of
primate foraging: red colobus of Kibale National Park. American Journal of
Physical Anthropology. 117:349-363.
Chapman C. A., L.J. Chapman, K. Vulinec, A. Zanne, and M.J. Lawes. 2003a. Biotropica
35:382-393.
Chapman C.A. and J. Lambert. 2000. Habitat alteration and the conservation of African
primates: a case study of Kibale National Park, Uganda. American Journal of
Primatology 50:169-185.
Chapman C. A., M.J. Lawes, L. Naughton-Treves, and T.R. Gillespie. 2003b. Primate
survival in community-owned forest fragments: are metapopulation models useful
amidst intensive use? Pp. 63-78, in L.K. Marsh, ed. Primates in Fragments: Ecology
and Conservation. Kluwer Academic/Plenum Publishers, New York.
Chapman C. A. and D.A. Onderdonk. 1998. Forests without primates: primate/plant
codependency. American Journal of Primatology 45:127-141.
Chapman C.A. and C.A. Peres. 2000. Primate conservation in the new millenium: the
role of scientists. Evolutionary Anthropology 10:16-33.
Chiarello A.G. 2000. Density and population size of mammals in remnants of Brazilian
Atlantic forests. Conservation Biology 14:1649-1657.
Collias N. and C. Southwick. 1952. A field study of population density and social
organization in howling monkeys. Proceedings of the American Philosophical
Society 96:143-156.
Coombs I. and D.W.T. Crompton. 1991. A Guide to Human Helminths. Taylor and
Francis, London.
Coop R.L. and P.H. Holmes. 1996. Nutrition and parasite interaction. International
Journal of Parasitology 26:951-962.


Copyright 2004
by
Thomas R. Gillespie


3
Chapman 2000). Thus, forest fragmentation appears to negatively impact most primate
communities and species.
The impact of selective logging on primate populations depends greatly on the
intensity of the logging and the species in question. Low-intensity logging (5-20% of
trees destroyed) appears to be compatible with primate conservation (Johns and Skorupa
1987; Ganzhom 1995; Oates 1996; Brugiere 1998; Chapman et al. 2000). For example,
Ganzhom (1995) determined that low-intensity logging of forests in Madagascar
(affecting less than 10% of forest area) corresponds with an increase in abundance of all
lemur species (significantly so for three of seven species). Moreover, studies from
Kibale National Park in Uganda demonstrate that primate densities in low-intensity
logged forest are no different from primate densities in unlogged forest (Skorupa 1988;
Chapman et al. 2000). Consequently, low-intensity, selective logging potentially offers a
land-use option compatible with primate conservation.
In contrast, high-intensity logging (>50% of trees destroyed), the most common
form of logging in the tropics, appears to be detrimental to most primate populations
(Skorupa 1988; Bennett and Dahaban 1995; Chapman et al. 2000). For example, Bennett
and Dahaban (1995) found that high-intensity logging resulted in a 35-70% decline in
gibbon (Hylobates muelleri) and langur (Presbytis sp.) populations in Sarawak. Skorupa
(1988) demonstrated that 12 years after high-intensity logging, group densities of red
colobus (Piliocolobus tephrosceles) and red-tail guenons (Cercopithecus ascanius) were
lower compared to those in unlogged forest at Kibale National Park, Uganda. Chapman
et al. (2000) reveals that even 28 years after logging in the system examined by Skorupa
(1988), red-tail group densities were still lower in high-intensity logged forest compared


44
addition, nutrient content varies more among food items for guenons compared to
colobines at Kibale (K. Rode, personal communication). Thus, variation in nutritional
condition is likely more sensitive to changes in habitat for guenons than for colobines.
Parasite infections are common in nature and low-intensity infections are often
asymptomatic. Endemic stability is common, resulting in coexistence of parasite, vector
(in vector-borne parasites), host, and environment such that clinical disease is rare
(Norval et al 1992). However, anthropogenic change may result in a loss of endemic
stability associated with altered vector dynamics, transmission rates, parasite host range,
and parasite virulence (Deem et al. 2001). Resultant high-intensity infections, as well as
moderate-intensity infections in stressed animals, can result in morbidity and mortality.
Comparisons of parasite prevalence can be a useful indirect indicator that parasites
may be impacting host populations (i.e., population declines correlated to increased
infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting
guenons at higher prevalence in the logged forests have the capacity to cause substantial
pathology and death in primates (Table 4-1). Heavy infections of Oesophogostomum sp.,
Strongyloides sp., and Enterobius sp. are associated with mucosal inflammation,
ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and
Johnsen 1978; Holmes et al. 1980; Harper et al. 1982; Liu et al. 1995; Murata et al.
2002). Even moderate intensities of Oesophogostomum sp. have proven clinically
important in stressed captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For
example, nearly 30% of 70 guenons imported to Italy from Senegal died soon after
arrival from severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial
infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent


16
Kenya than in Uganda, and higher in Uganda than in South Africa (X2 = 64.03, P <
0.001). Strongyloides sp. prevalence was higher in blue monkeys in Kenya compared to
those in Uganda and South Africa (X2 = 93.85, P < 0.001). Prevalence of
Streptopharagus sp. in blue monkeys was higher in South Africa than in Kenya, and
prevalence in Kenya was higher than in Uganda (X2 = 54.66, P < 0.001). Infections of an
anoplocephalid, thought to be Bertiella sp., were documented for blue monkeys in South
Africa and Uganda and prevalence was higher in blue monkeys in South Africa compared
to those in Uganda (X2 = 32.35, P < 0.001).
McGrew et al. (1989) reported on the gastrointestinal parasites of vervet monkeys
in Senegal. Although Trichuris sp. infections were not documented, and another
spiruroid nematode, Physaloptera sp., replaced Streptopharagus sp.; the overall helminth
fauna was similar to that of vervets in my study.
Discussion
To my knowledge, this is the first report of gastrointestinal helminth parasites from
wild populations of redtail guenons and l'hoesti monkeys, and the first report of
gastrointestinal helminth parasites from blue and vervet monkeys from Uganda.
The similarities in gastrointestinal parasite faunas among the guenons of western
Uganda suggest that generalist parasites predominate, supporting the contention that in
communities comprised of closely related species (i.e., Cercopithecus spp.), cross-species
interaction may be an important source of infection risk (Ezenwa 2003). This may be one
reason why redtail guenons associate with unrelated red colobus monkeys far more than
with other guenon species (Chapman and Chapman 2000).
Seasonal patterns of infection were not readily apparent for any of the parasite
species infecting redtail guenons. This result is unexpected, as previous studies of


72
stumps/ha, red colobus/ha, and total colobines/ha. The size of each fragment was
measured, taking GPS readings at locations along fragment edges and/or measuring
fragment perimeters with a 50 m tape (Onderdonk and Chapman 2000). Fragments were
classified as crater lake, hillside, or valley bottom. Crater lake and hillside fragments (n
= 4) were forests on steep hills or sides of explosion craters; for analyses, they are
considered together. Valley-bottom fragments (n = 5) have swamp vegetation associated
with their lowest levels. Consequently, valley-bottom fragments may retain greater
humidity, potentially providing a better environment for the development of strongyle
nematodes during their free-living stage. Distance to Kibale National Park and nearest
fragment are straight-line distances measured from topographic maps. At each fragment,
all trees > 10 cm DBH (Diameter at Breast Height; Chapman et al. 2003) were identified
and measured. Sizes of trees on very steep craters were visually estimated (error in visual
estimation = + 3.7%, N = 46). As colobus rarely feed in small trees (Gillespie and
Chapman 2001), this represents a nearly complete inventory of all colobus potential food
sources. Tree stumps remaining after harvest by local people were also counted. This
involved carefully searching through vine tangles and dense herbaceous vegetation in
search of hidden stumps. For most tree species, the stump will remain for several years,
providing an index of habitat degradation.
Since parasite dynamics could be influenced by host density, the density of red
colobus and black-and-white colobus (Colobus guereza) were determined via
observations made over 24-hours at each fragment. I include red colobus, as well as total
colobus, density among biological attributes examined, since black-and-white colobus
may serve as a reservoir host for red colobus infection with shared parasites.


Forest Fragmentation
Reduced Tree Density G Diversity
Reduced Habitat Area
Reduced Food Availability
Increased Contact with
Humans G Livestock
Restricted Ranging
y
Crowding Chronic Stress
Introduction of Novel Pathogens
y
Population Declines
Figure 5-1. Conceptual model of proposed mechanism for population declines in forest


LIST OF REFERENCES
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Ashford R.W., G.D.F. Reid, and R.W. Wrangham. 2000. Intestinal parasites of the
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Bennett E.L. and Z. Dahaban. 1995. Wildlife responses to disturbances in Sarawak and
their implications for forest management. Pp. 66-86 in R.B. Primack and T.E.
Lovejoy, eds. Ecology, Conservation, and Management of Southeast Asian
Rainforests. Yale University Press, New Haven, CT.
82


Table 4-2. Prevalence (%) of gastrointestinal parasite infections in redtail guenons (Cercopithecus ascanius) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Logged(n = 235)
Undisturbed (n = 35)
Significance
Trichuris sp.
63
21
***
Streptopharagus sp.
32
13
*
Strongyloides fulleborni
16
4
**
Oesophagostomum sp.
21
3
***
Enterobius sp.
5
0
N.A.
Dicrocoeliid liver fluke
11
0
N.A.
Bertiella sp.
3
0
N.A.
Giardia lamblia
26
0
N.A.
Entamoeba coli
26
5
***
Entamoeba histolytica
26
5
***
Chilomastix mesnili
8
0
N.A.
Iodameoba buetschlii
26
5
***
Overall
92
29
***
* P < 0.05, ** P < 0.01, *** P < 0.001, N.A. no chi-square test performed since one forest type had 0 prevalence


Table 6-1. Physical and biological attributes of forest fragments with red colobus (Piliocolobus tephroceles) populations near Kibale
National Park, Uganda
Fragment
Size (ha)
Fragment
Type
Distance to
Kibale (km)
Nearest
Fragment (m)
Trees/ha
Tree species/ha
Stumps/ha
Red Colobus/ha
Colobines/ha
Bugembe
4.68
VB
2.5
500
52
8.76
71.18
2.35
2.35
CK
8.70
HS
0.2
150
41
4.94
45.75
2.87
3.68
Kifuruka
7.24
CL
6.5
95
27
4.03
12.42
0.55
1.66
Kiko 1
6.20
VB
2.0
50
42
6.61
56.45
3.55
4.19
Kiko 2
5.00
VB
1.8
125
63
4.00
8.40
2.80
5.20
Kiko 3
1.70
VB
1.1
70
231
12.94
221.76
4.71
9.41
Kiko 4
1.20
VB
1.1
70
259
20.83
174.17
8.33
8.33
Nkuruba
6.40
CL
3.6
70
445
73.00
0.16
3.44
6.72
Rutoma
4.90
HS
3.0
150
34
7.76
32.24
4.69
8.16
Average
5.11
N.A.
2.4
142
133
15.87
69.17
3.70
5.52


25
Strongyloides stercoralis was identified based on larvae size and morphology
(rhabditiform esophagus, prominent genital primordium, and short buccal cavity).
Strongyloides stercoralis larvae were found only in the feces of red colobus, and
measured 242.4 4.5 pm in length.
Superfamily Ascaroidea: Ascaris sp. was identified based on egg size and
morphology (round or oval, thick-shelled, brown or yellow brown, and mammillated
albuminous covering). Eggs were found in feces of red colobus and eastern black-and-
white colobus, and measured 65.2 1.3 X 55.8 1.1 pm and 63.9 1.4 X 54.4 1.0 pm,
respectively. Prevalence of Ascaris sp. was higher for eastern black-and-white colobus
than for red colobus (X2 = 10.71, d.f. = 1, P < 0.005, Table 3-1).
Superfamily Oxyuroidea: Colobenterobius sp. was identified based on egg size
and morphology (elliptical and thick-shelled) from red colobus and eastern black-and-
white colobus and and verified by adults obtained by necropsy. Colobenterobius sp. eggs
were found in the feces of red colobus and eastern black-and-white colobus, and
measured 64.8 1.6 X 36.4 1.4 pm and 65.3 1.2 X 36.6 1.6 pm, respectively.
Prevalence of Colobenterobius sp. did not differ between colobus species (P > 0.1, Table
3-1). This parasite is more reliably diagnosed by examination of peri-anal skin or by
necropsy (Ashford et al. 2000). Consequently, these prevalence values are likely an
underestimation of prevalence.
Cestoda
Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed
oncosphere) were found in feces of red colobus and eastern black-and-white colobus, and
measured 40.3 0.8 X 48.8 1.2 pm and 41.2 1.4 X 50.0 1.0 pm respectively. No
proglottids were detected through macroscopic inspection of feces. Prevalence of


2
novel diseases. My study addresses an important aspect of these questions by examining
the effects of selective logging and forest fragmentation on primate-parasite dynamics in
an African tropical forest.
To provide background information on the framework of the research, this
introduction reviews the patterns of human disturbance and their impacts on primate
populations. Little is known about the mechanisms by which human disturbance impacts
primate populations and ecosystem processes. My study examines one potential
mechanism, primate-parasite dynamics. Since it is likely that pathogens and other factors
interact to produce an effect on primate populations, I provide background on human
disturbance and primate populations, and discuss how this may relate to primate-parasite
dynamics. This is followed by the objectives, rationale, methodology, and research
implications of my work.
Human Disturbance and Primate Populations
Forest fragmentation and selective logging dominate habitat-modification patterns
throughout the tropics (Chapman et al. 2000; Chapman and Peres 2001) and have
detrimental effects on most primate populations (Skorupa 1988; Bierregaard et al. 1992;
Bennett and Dahaban 1995; Chapman et al. 2000; Onderdonk and Chapman 2000). With
respect to forest fragmentation, primate species richness is lower in forest fragments
compared to equivalent areas of continuous forest (Bierregaard et al. 1992; Onderdonk
and Chapman 2000); primate species richness is typically higher in large compared to
small fragments (Bierregaard et al. 1992; Estrada et al. 1994; but see Onderdonk and
Chapman 2000); and primate densities typically are higher in large compared to small
fragments (Estrada and Coates-Estrada 1996; Chiarello 2000; but see Onderdonk and


6
1998). Each of these epidemics was potentially anthropozoonotic, meaning that the apes
were potentially infected by contact with humans. Yellow fever was implicated as the
cause of a 50% decline in the howling monkey (Alouatta palliata) population on Barro
Colorado Island, Panama, between 1933 and 1951 (Collias and Southwick 1952). Later
studies of this same howling monkey population suggested that heavy botfly infestations
(Alouattamyia baeri), in conjunction with food limitation, were limiting monkey densities
(Smith 1977; Milton 1996). Interestingly, Barro Colorado Island was isolated from a
much larger area of continuous disturbed forest after the damming of Lake Gatun during
the formation of the Panama Canal, and is hence the result of large-scale human
disturbance. The predominance of cases of population-level effects of parasites on
primates from human-disturbed systems suggests that populations in disturbed habitats
may be more vulnerable to parasites. However, more studies will be needed to confirm
this, since few studies have expressly looked at such issues in undisturbed systems.
Disturbance and Primate-Parasite Dynamics
The direct pathological effects and accompanying reduction in host condition
resulting from parasitic infections may play a role in the lower abundance and species
richness of primate communities in disturbed systems. While reproductively active
primate groups may be sustained in forest fragments and selectively logged forests, little
is known about the effects of such disturbance on primate health. These disturbance
regimes result in changes in forest structure and climate, increased human presence, and
decreased food availability (Kapos 1989; Williams-Linera 1990; Laurance et al. 1996;
Didham and Lawton 1999; Chapman et al. 2000; Chapman and Peres 2001). Such
changes may increase or decrease the likelihood of parasite infection. Forest fragments
have consistently lower canopy height and higher foliage density than continuous forest


91
Lilly A.A., P.T. Mehlman, and D. Doran. 2002. Intestinal parasites in gorillas,
chimpanzees, and humans at Mondika Research Site, Dzanga-Ndoki National Park,
Central African Republic. International Journal of Primatology 23:555-573.
Liu L.X., J. Chi, M.P. Upton, and L.R. Ash. 1995. Eosinophilic colitis associated with
larvae of the pinworm Enterobius vermicularis. Lancet 346:410-412.
Lloyd S. 1998. Other cestode infections: hymenolepiosis, diphyllobothriosis, coenurosis
and other larval and adult cestodes. Pages 635-649 in S.R. Palmer, L. Soulsby, and
D.I.H. Simpson, editors. Zoonoses. Oxford University Press, Oxford.
LoGuidice K., R.S. Ostfeld, K.A. Schmidt, and F. Keesing. 2003. The ecology of
infectious disease: Effects of host diversity and community composition on Lyme
disease risk. Proceedings of the National Academy of Science 100:567-571.
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Wildlife Medicine 24:315-326.
Malcolm J.R. 1994. Edge effects in central Amazonian forest fragments. Ecology 75 (8):
2438-2445.
Marsden S.J. 1998. Changes in bird abundance following selective logging on Seram,
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Marsh L.K. 2003. Primates in fragments: ecology and conservation. Kluwer
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B 269: 2041-2049.


36
of the park at an elevation of 1,500 m (Gillespie and Chapman 2001). Kanyawara
experiences a bimodal pattern of seasonal rainfall, with peaks occurring in March-May
and August-November. Mean annual rainfall (1990-2001) is 1,749 mm (Chapman et al.
2002). Daily temperature minima and maxima averaged 14.9C and 20.2C,
respectively, from 1990 to 2001.
Prior to becoming a National Park in 1993, Kibale was a Forest Reserve, gazetted
in 1932 with the stated goal of providing a sustained production of hardwood timber
(Osmaston 1959). A polycyclic felling cycle of 70 years was initiated, and it was
recommended that logging open the canopy by approximately 50% through the harvest of
trees> 1.52 m in girth (Kingston 1967). This history of logging has led to varying
degrees of disturbance among sites. I conducted my study in two forestry compartments;
one logged at high intensity in the late 1960s (K-15), and one undisturbed (K-30).
The K-15 forestry compartment is a 347-ha section of forest that experienced high-
intensity, selective felling from September 1968 through April 1969. Total harvest
averaged 21 m3/ha or approximately 7.4 stems/ha (Struhsaker 1997), but incidental
damage was much higher. It is estimated that approximately 50% of all trees in
compartment K-15 were destroyed by logging and incidental damage (Skorupa 1988). A
total of 18 tree species were harvested, with nine species contributing more than 95% of
the harvest volume (Kasenene 1987; Skorupa 1988). Many of the tree species harvested
provided primates with food (Struhsaker 1997; Chapman et al. 2000).
The K-30 forestry compartment is a 282-ha area that has not been commercially
harvested. Prior to 1970, however, a few large stems (0.03-0.04 trees/ha) were removed
by pitsawyers. This extremely low level of extraction seems to have had little effect on


45
complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of
all parasites infecting guenons in logged forests at Kibale may contribute to greater
morbidity and mortality in this guenon population compared to the population inhabiting
undisturbed forests.
The magnitude and prevalence of multiple-species infections in individuals can be
another useful indirect indicator that parasites may be impacting host populations.
Multiple-species infections are associated with a greater potential for morbidity and
mortality due to synergistic and competitive interactions occurring between parasite
species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sebelis 1995).
For example, concurrent infections with Heligmosomoides polygurus and Trypanosoma
congolense in mice (Fakae et al. 1994) and Escherichia coli and Ascaris suum in pigs
(Adedeji et al. 1989) result in higher mortality than single infections. Similarly, in
humans, Schistosoma, mansoni has an increased effect on the development of
malnutrition in the presence of T. trichiura (Parraga et al. 1996) and a range of parasites
demonstrate greatly elevated pathogenic effects in the presence of HIV (Gomez et al.
1995; Kaplan et al. 1996). Consequently, the elevated frequency and number of multiple-
species infections observed in guenons in logged forests at Kibale may contribute to
greater morbidity and mortality in this guenon population compared to the population
inhabiting undisturbed forests.
Other dietary differences between guenon and colobine species may also play a role
in the patterns observed. Encounter probabilities for some of the parasites involved
would be expected to differ between guenons and colobines. Bertiella sp., Dicrocoelium
sp. and Streptopharagus sp. have intermediate hosts. Guenons feed on many of these


15
Protozoa
Cysts of 3 amoebae and 2 flagellates were identified from 235 fecal samples from
redtail guenons. Cysts most closely resembling Entamoeba coli were multinucleate, with
a mean diameter of 17.8 1.1 pm. Cysts most closely resembling Entamoeba histolytica
had a mean diameter of 12.9 2.1. Cysts most closely resembling Iodameoba butschlii
had a single nucleus, distinct glycogen vacuole, and a mean diameter of 11.2 2.1. Cysts
most closely resembling Giardia lamblia were ovoid with a mean diameter of 11.4 1.4.
Cysts most closely resembling Chilomastix mesnili were lemon-shaped, with a mean
diameter of 7.5 1.1. Prevalence in redtail guenons was relatively low for all
protozoans; Entamoeba coli (11%), Entamoeba histolytica (10%), Iodameoba butschlii
(10%), Giardia lamblia (4%), and Chilomastix mesnili (1%).
Effect of Season and Host Sex on Infection Prevalence
While prevalence did not correlate with monthly rainfall for any parasite species
infecting redtail guenons (P > 0.496), seasonal fluctuations did occur (Figure 2-1).
Although prevalence did not differ between male (n = 12) and female (n = 98) redtail
guenons for any shared parasite species (P > 0.05), Oesophagostomum sp. (n = 24) and S.
fulleborni (n = 16) infections were only detected in adult females.
Variation in Prevalence among Sites throughout Africa
Previous studies have investigated the gastrointestinal parasites of blue monkeys
from South Africa (Appleton et al. 1994) and Kenya (Munene et al. 1998). Comparisons
with my study demonstrate great similarity in helminth faunas of blue monkeys among
sites. However, prevalence varied greatly among sites. Trichuris sp. prevalence was
lower in blue monkeys in Uganda compared to those in Kenya and South Africa (X2 =
11.96, P < 0.005). Prevalence of Oesophagostomum sp. in blue monkeys was higher in


CHAPTER 4
LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN AFRICAN
PRIMATE POPULATIONS
Introduction
With few areas legally protected from human exploitation, the conservation of
many species will depend on the capacity of disturbed areas to support their populations.
Knowledge of how particular species are affected by specific forms of anthropogenic
environmental change is essential for developing sound conservation and management
plans, as well as assessing the relative conservation value of various disturbed habitats.
Selective logging is a dominant habitat disturbance pattern with strong conservation
potential (Frumhoff 1995; Struhsaker 1997; FAO 1999; Chapman and Peres 2001). A
multitude of studies have examined the effects of selective logging on the abundance and
diversity of invertebrate (Willott et al. 2000; Lewis 2001; Summerville and Crist 2002;
Hamer et al. 2003) and vertebrate taxa (Johns and Skorupa 1987; Johns 1992; Heydon
and Bulloh 1997; Marsden 1998; Robinson and Robinson 1999). Although logging often
results in a reduction in overall diversity, effects on individual species are difficult to
predict. The nature and intensity of response appear to vary depending on species and
site characteristics. For example, following heavy logging at Kibale National Park in
Uganda, red colobus monkeys (Piliocolobus tephroceles) declined, while black-and-
white colobus monkeys (Colobus guereza) increased in density (Chapman et al. 2000).
Another primate, the blue monkey (Cercopithecus mitis) declined after logging at Kibale,
32


95
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Parraga I.M., A.O. Assis, and M.S. Prado. 1996. Gender differences in growth of school-
aged children with schistosomiasis and geohelminth infection. American Journal of
Tropical Medicine and Hygiene 55:150-156.
Patz J.A., T.K. Graczyk, N. Geller, and A.Y. Vittor. 2000. Effects of environmental
change on emerging parasitic diseases. International Journal for Parasitology.
30:1395-1405.
Peres C.A. 1990. Effects of hunting on Western Amazonian primate communities.
Biological Conservation 54:47-59.
Phillippi K.M. and M.R. Clarke. 1992. Survey of parasites of rhesus monkeys housed in
small social groups. American Journal of Primatology 27:293-302.
Plumptre A.J. and V. Reynolds. 1994. The effect of selective logging on the primate
populations in the Budongo Forest Reserve, Uganda. Journal of Applied Ecology
31:631-641.
Pit D.S.S., J. Bloktkamp, A.M. Polderman, S. Baeta, and M.L. Eberhard. 2000. The
capacity of the third-stage larvae of Oesophagostomum bifurcum to survive adverse
conditions. Annals of Tropical Medicine and Parasitology 94:165-171.
Poulin R. 1998. Evolutionary Ecology of Parasites: From Individuals to Communities.
Chapman and Hall, London.
Pussey A. 1998. Scabies in chimpanzees of Gombe National Park, Tanzania. European
Association of Zoo and Wildlife Veterinarians-Newsletter 1:10.
Redford K.H. 1992. The empty forest. Bioscience 42:412-422.
Rigby M.C. and Y. Moret. 2000. Life-history trade-offs with immune defenses. Pages
129-142 in R. Poulin, S. Morand, and A. Skorping, editors. Evolutionary biology of
host-parasite relationships: theory meets reality. Elsevier Science, Amsterdam.
Robinson J.G. and E.L. Bennett. 2000. Carrying capacity limits to sustainable hunting in
tropical forests. Pages 13-30 in J.G. Robinson and E.L. Bennett, editors. Hunting
for sustainability in tropical forests. Columbia University Press, New York.
Robinson W.D. and S.K. Robinson. 1999. Effects of selective logging on forest bird
populations in a fragmented landscape. Conservation Biology 13:58-66.
Roperto F., A. Queseda, F. Pandolfi and R. Izzi. 1985. Oesophagostomiasis in monkeys
imported from Senegal. Atti delle Societa Italiana delle Scienze Veterinairie
38:603-605.


18
The helminth fauna of vervets was similar between Uganda and Senegal (McGrew
et al. 1989). However, small sample size precluded comparisons of prevalence.
Freeland (1977) reported on the protozoan parasites of several primate species in
Kibale National Park. His study identified 2 protozoans from redtail guenons not found
in our study (i.e., Entamoeba hartmanni and an unidentified flagellate). Although
Freeland (1977) does identify Chilomastix mesnili cysts from several species, they were
not identified from redtail guenons. Despite these differences, the overall protozoan
fauna of redtail guenons reported by Freeland (1977) and my study were similar.
Unfortunately, Freeland (1977) does not provide data on prevalence.
My study contributes baseline data on the patterns of parasitic infection in wild
guenons, providing a first step toward an index of population health and disease risk
assessment for conservation and management plans of threatened guenon populations.
My study also reveals that many of the gastrointestinal parasites of the guenon species
examined may be zoonotic. Accordingly, future studies are needed to determine risks of
cross-transmission. Mechanisms to reduce such risks would promote human health,
livestock production, and local support for conservation.
Gastrointestinal parasite classification by fecal analyses is weak by its very nature.
However it is the only responsible method to approach threatened species. Future studies
employing molecular analyses and opportunistic necropsies are needed to improve our
classification of the gastrointestinal parasites of guenons, and to improve our
understanding of the risks of epizootic and zoonotic transmission.


CHAPTER 2
GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN UGANDA
Introduction
The guenons, Cercopithecus spp., are the most diverse taxa of primates endemic to
sub-Saharan Africa (Grubb et al. 2002). These frugivorous monkeys live in groups of 10-
30 individuals and often form mixed-species associations with other primate species
(Chapman and Chapman 2000). Although guenons can be found in a wide variety of
habitats, the majority inhabit tropical forests (Butynski 2002). More than two-thirds of
sub-Saharan Africas original forest cover has been lost because of anthropogenic
disturbance (World Resources Institute 1998), and forest cover continues to decline at a
rate of 0.7% annually (FAO 1999). Due largely to resultant habitat loss, 26% of guenons
are endangered (Butynski 2002).
Although parasite infections are common in nature and low-intensity infections are
often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic
change may result in a loss of stability associated with altered transmission rates, host
range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline
data on patterns of parasitic infections in wild guenon populations are critical to provide
an index of population health, and to begin to assess and manage disease risks.
Although many studies have documented the gastrointestinal parasites of wild
populations of African apes (Huffman et al. 1997; Graczyk et al. 1999; Nizeyi et al. 1999;
Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et al.
1989; Miiller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other
10


75
low stump density (Kiko 3 mean = 3.33 0.64 larvae/m3, Nkuruba mean = 0.82 0.98
larvae/m3, t= -2.87, P = 0.005). However, Oesophagostomum sp. L3 larvae were not
found in canopy or soil plots.
Discussion
The results of this study demonstrate that an index of habitat degradation, stump
density, best explained the prevalence of strongyle and rhabditoid nematode infections in
red colobus in forest fragments in western Uganda. I also found a greater risk of
infection with Oesophagostomum sp., a representative strongyle, for red colobus in the
fragment with the highest stump density compared to the fragment with the lowest stump
density. In some cases, fragment size and colobine density were also related to strongyle
and rhabditoid prevalence, but these variables did not explain a significant amount of
variation that was independent of stump density.
These results may provide insights into observed declines in red colobus in the
forest fragments of western Uganda. As noted earlier, red colobus declined in these
forest fragments by 20% between surveys in 2000 and 2003. Altered parasite dynamics
may play a role in these declines. Although parasite infections are common in nature and
low-intensity infections are often asymptomatic (Anderson and May 1979; May and
Anderson 1979), anthropogenic change may result in altered transmission rates, parasite
host range, and parasite virulence (Daszak et al. 2000; Patz et al. 2000). Resultant
changes in host susceptibility may result in elevated morbidity and mortality, and
ultimately, population declines.
The strongyle and rhabditoid nematodes documented to infect red colobus in this
study have the capacity to cause substantial pathology and death in primates. Heavy
infections of Oesophogostomum spp. and Strongyloides spp. have been associated with


76
mucosal inflammation, ulceration, dysentery, weight loss, and death in primates
(McClure and Guilloud 1971; DePaoli and Johnsen 1978; Holmes et al. 1980; Harper et
al. 1982). Even moderate intensities of Oesophagostomum sp. have proven important in
stressed or captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For example,
nearly 30% of 70 guenons imported to Italy from Senegal died soon after arrival from
severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial infections of
mucosal lesions resulting in ulceration and fatal septicaemia are frequent complications
of oesophogostomiasis (Soulsby 1982). Even more troubling are S. stercoralis and
unidentified strongyle infections, which are likely anthropozoonotic in origin. These
parasites occur at high frequency in the human populations in the region, but are absent
from colobus within Kibale National Park, where the people and primates interact at a
reduced frequency. Since S. stercoralis parasitic females live in the superficial tissues of
the small intestine, and can be present in high numbers due to autoinfection, they can
cause significant pathology in humans (Pappas and Wardrop 1999).
Considering the potential role that strongyle and rhabditoid nematode infections
may play in red colobus declines in forest fragments, we should investigate ways to
mitigate alterations in infection dynamics in the face of extraction.


43
1997). In addition, at both 22 and 32 years post-logging, the basal area of trees in logged
forests was less than in undisturbed forests (Chapman and Chapman, in press). Thus, a
primary guenon food resource, mature fruit-bearing trees, were reduced significantly in
density by logging and young trees are not successfully regenerating to replace those lost
to logging. Consequently, it is not surprising that red colobus have begun to recover in
parallel with their food resources; while guenons have not recovered.
Although food availability accounts well for the lack of recovery in guenon
populations in logged forests, it is not clear why populations are declining. However,
nutrition and parasite dynamics may interact to play a role in these declines. Correlations
among elevated parasitism, reduced nutrition, and reduced body condition are well
documented (Mori 1979, Eley et al. 1989; Gulland 1992; Milton 1996); however,
causation remains equivocal. Milton (1996) demonstrated that howler monkey (Alouatta
palliata) mortality was best explained by the interaction of age, physical condition,
dietary stress, and intensity of parasitic bot fly infestations. Similarly, Gulland (1992)
found that the timing of population crashes in Soay sheep (Ovis aries) were strongly
correlated with emaciation, high intensity nematode infections, and signs of protein-
energy malnutrition. Moreover, free-ranging sheep treated with antihelminthics had
lower mortality rates, while experimentally infected sheep fed nutritious diets showed no
sign of malnutrition. Recent evidence from Kibale indicates that dietary stress affects
redtail guenons in logged forests. These guenons have lower intake of crude protein and
the majority of key minerals compared to guenons in undisturbed forests (K. Rode,
personal communication). Such protein deficiencies have been linked to depressed
immune function (Chandra 1983; Bundy and Golden 1987; Koski and Scott 2001). In


Table 5-2. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from forest fragments
and undisturbed forests in Kibale National Park, Uganda
Parasite Species
Fragmented (n = 94)
Undisturbed (n = 106)
Significance
Trichuris sp.
90
84
N.S.
Unidentified strongyle
5
0
N.A.
Strongyloides fulleborni
7
3
N.S.
Oesophagostomum sp.
4
9
N.S.
Asear is sp.
6
0
N.A.
Entamoeba coli
6
9
N.S.
Entamoeba histolytica
5
9
N.S.
Overall
90
84
N.S.
N.S.p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence


74
but it ranged from 0 to 12. Collectively, the prevalence of strongyles and rhabditoids was
20% and ranged from < 1% to 68%.
Individually and collectively, the prevalence of all strongyle and rhabditoid
nematodes was positively correlated with stump density (Table 6-3). With the exception
of Oespohagostomum sp., prevalence of all strongyles and rhabditoids individually and
collectively, was negatively correlated with fragment size (Table 6-3). Strongyloides
stercoralis prevalence was positively correlated with red colobus and total colobine
density (Table 6-3).
When predicting strongyle and rhabditoid prevalence using a step-wise multiple
regression that included stump density, fragment size, and colobus density; stump density
entered the model first explaining 85% of the variance (F = 38.84, R = 0.847, P < 0.001).
Subsequently, no other variable entered the model suggesting that fragment degradation,
indexed by stump density, was the most important variable in predicting strongyle and
rhabditoid prevalence and once this variable was considered, there was little remaining
variance that could be explained by other variables measured. Stump density was
correlated with fragment size (r=-0.811, P= 0.008), and colobus density (r=0.657,
P-0.054).
A similar situation was found when predicting Oespohagostomum sp. (F = 13.41,
R2 = 0.608, P = 0.008), S. fulleborni (F = 21.64, R2 = 0.756, P = 0.002), S. stercoralis (F
= 71.66, R2 = 0.911, P < 0.001), and the unidentified strongyle prevalence (F = 9.93, R2 =
0.587, P = 0.016), in that only stump density entered the model.
Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots
from Kiko 3, the fragment with high stump density, compared to Nkuruba, which had


Table 4-3. Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus tephroceles) from logged and undisturbed
forests in Kibale National Park, Uganda
Parasite Species
Logged(n =127)
Undisturbed (n = 561)
Significance
Trichuris sp.
40
36
N.S.
Strongyloides fulleborni
1
4
N.S.
Oesophagostomum sp.
5
2
N.S.
Colobenterobius sp.
0
1
N.A.
Entamoeba coli
6
3
N.S.
Entamoeba histolytica
6
3
N.S.
Overall
45
37
N.S.
N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence


Table 3-1. Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys of Uganda
Parasite Species Piliocolobus tephroceles in = 1,608)
Colobus suereza in = 476)
Colobus ansolensis in =19)
Strongyloides fulleborni
4
4
5
Strongyloides stercoralis
< 1
0
0
Oesophagostomum sp.
3
6
0
Unidentified strongyle
2
1
11
Asear is sp.
< 1
1
0
Trichuris trichiura
38
79
1
Colobenterobius sp.
< 1
1
0
Bertiella sp.
< 1
< 1
0
Dicrocoelium sp.
< 1
1
0
Entamoeba coli
4
8
16
Entamoeba histolytica
3
8
11
Giardia lamblia
1
0
0
Overall
38
79
100


73
Results
Mean fragment size for the 9 fragments surveyed was 5.11 ha and fragments ranged
from 1.20 to 8.70 ha (Table 6-1). Five of the fragments were classified as valley bottom
and 4 were crater lake or hillside (Table 6-1). Mean distance to Kibale National Park was
2.4 km and ranged from 0.2 to 6.5 km (Table 6-1). Mean distance to the nearest fragment
was 142 m and ranged from 50 (the criteria for a isolated fragment) to 500 m (Table 6-1).
Mean tree density was 133 trees/ha and ranged from 27 to 445 trees/ha (Table 6-1).
Mean tree species/ha was 15.9 tree species/ha and ranged from 4 to 73 tree species/ha
(Table 6-1). The level of degradation of the fragments was highly variable and stump
density ranged from 0.16 to 221.76 stumps/ha and averaged 69.2 stumps/ha (Table 6-1).
Stumps density reflects the intensity of extraction in these fragments, which was
associated with beer brewing, gin distillation, and charcoal production by households
bordering a fragment (Chapman et al 2003). Red colobus density averaged 3.70 red
colobus/ha and ranged from 0.55 to 8.33 red colobus/ha (Table 6-1). Mean colobine
density (red colobus and black-and-white colobus) was 5.52 colobines/ha and ranged
from 1.66 to 9.41 colobines/ha (Table 6-1).
Two strongyle (Oespohagostomum sp. and an unidentified strongyle) and 2
rhabditoid nematodes (Strongyloides fulleborni and S. stercoralis) were found from red
colobus inhabiting forest fragments (Table 6-2). Mean prevalence among fragments of
Oespohagostomum sp. was 5%, but prevalence ranged from 0 to 24 %. Mean prevalence
of the unidentified strongyle was 8% and ranged from 0 to 28%. S. fulleborni prevalence
averaged 6% among fragments and ranged from 0 to 16%. The prevalence of S.
stercoralis was the lowest of all nematodes examined averaging 2% among fragments,


Table 5-1. Prevalence (%) of gastrointestinal parasite infections in red colobus {Piliocolobus tephroceles) from forest fragments and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Fragmented (n = 390)
Undisturbed (n = 561)
Significance
Trichuris sp.
50
36
***
Unidentified strongyle
6
0
N.A.
Strongyloides fulleborni
5
4
N.S.
Strongyloides stercoralis
2
0
N.A.
Oesophagostomum sp.
4
2
*
As caris sp.
< 1
0
N.A.
Colobenterobius sp.
< 1
1
N.S.
Bertiella sp.
< 1
0
N.A.
Entamoeba coli
13
3
***
Entamoeba histolytica
10
3
**
Giardia lamblia
6
0
N.A.
Overall
50
37
***
* p < 0.05, ** p < 0.005, *** p < 0.001, N.S. p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence.


Conservation Society, and the Ford Foundation. Permission to conduct this research was
provided by the Uganda National Research Council, Office of the President, the Uganda
Wildlife Authority, and Makerere University.
This dissertation is dedicated to Brian Riewald, whose spirit and character will
always be with me.
IV


EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS
By
THOMAS R. GILLESPIE
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
2004


17
primate parasite infections from tropical forest sites have documented an increase in
prevalence during the rainy season (Freeland 1977; Huffman et al. 1997). It is difficult to
ascertain why seasonal differences were not seen in this study. However, fluctuation in
infection prevalence was high, warranting future investigation of the mechanism behind
these differences (Figure 2-1).
Although no differences in prevalence of infection were apparent between male and
female guenons for shared parasite species, only adult females were infected with
Oesophagostomum sp. and S. fulleborni. This may reflect energy and nutrient stress
associated with producing and raising infants, which may result in an increased
susceptibility to infection (Gulland 1992; Milton 1996).
Studies investigating the gastrointestinal parasites of blue monkeys, revealed
similar helminth faunas among sites (Appleton et al. 1994; Munene et al. 1998). This
might be expected because of the recent origin of blue monkeys (Leakey 1988; Ruvolo
1988). However, parasite prevalence varied greatly among sites. In general, helminth
prevalence was highest for Kenyan blue monkeys (with the exception of Streptopharagus
sp., which had the highest prevalence for South African blue monkeys). In most cases,
intermediate prevalence was seen in Ugandan compared to Kenyan and South African
blue monkeys. Kenyan forests are small and fragmented, compared to those sampled in
Uganda and South Africa (Appleton et al. 1994); and evidence presented in later chapters
of this dissertation suggests that primates living in forest fragments may be more
susceptible to infection, and demonstrate higher prevalence compared to conspecifics
inhabiting large, undisturbed forests. This may explain the high prevalence of infection
in Kenyan blue monkeys compared to the other 2 sites.


Table 4-1. Mode of infection, morbidity, and mortality associated with gastrointestinal parasites infecting redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda
Parasite Species
Mode of Infection
Morbidity/Mortality
Sources
Trichuris sp.
Embryonated egg ingested
Typically asymptomatic
Beaver et al. 1984; Baskin 1993
Streptopharagus sp.
Intermediate host ingested
(cockroach, beetle)
Typically asymptomatic
Beaver et al. 1984; Coombs and
Crompton 1991
Strongyloides fulleborni
Larvae ingested, skin
Mucosal inflammation,
McClure and Guilloud 1971;
penetration
ulceration, death
Pampiglione and Ricciardi 1972
Oesophagostomum sp.
Larvae ingested
Severe diarrhea, weight loss,
death
Crestian and Crespeau 1975;
Roperto et al. 1985
Enterobius sp.
Egg ingested
Dysentary, enteritis, ulceration,
death
Liu et al. 1995; Murata et al. 2002
Colobenterobius sp.
Egg ingested
Dysentary, enteritis, ulceration,
death
Hugot 1999
Dicrocoeliid liver fluke
Metacercaria ingested in ant
or on vegetation
Typically asymptomatic
Beaver et al. 1984; Coombs and
Crompton 1991
Bertiella sp.
Cysticercoid ingested in
orbatid mite
Typically asymptomatic
Fiennes 1967; Lloyd 1998
Giardia lamblia
Cyst or trophozoite ingested
Typically asymptomatic,
possibly epizoonotic
Fiennes 1967; Baskin 1993
Entamoeba coli
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984
Entamoeba histolytica
Cyst or trophozoite ingested
Hepatic and gastric amoebiasis,
death
Loomis 1983
Chilomastix mesnili
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984
Iodameoba buetschlii
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984


68
(Chapman et al. 2003). While studies involving protected fragments have provided us
with many insights, they may have biased our perception of the value of forest fragments
for conservation.
Second, a number of simple logical predictions relating to primates in forest
fragments have not proven to be general. For example, home range size was frequently
cited as influencing a species ability to survive in a fragment (Lovejoy et al 1986; Estrada
and Coates-Estrada 1996). However, Onderdonk and Chapman (2000) found no
relationship between home range size and ability to live in fragments for a community of
primates in western Uganda. Similarly, it has been suggested that a highly frugivorous
diet may limit the ability of a species to live in fragments (Lovejoy et al 1986; Estrada
and Coates-Estrada 1996). However, Tutin et al. (1997) found that several frugivorous
species were at higher or similar densities in forest fragments than in the intact forest of
Lop Reserve, Gabon (see also Tutin 1999; Onderdonk and Chapman 2000).
Lastly, past studies have often focused on simple correlates to primate population
viability in forest fragments. However, finding such single correlative explanations for
complex biological phenomena, like determinants of primate abundance in fragments, is
unlikely. Rather, recent long-term studies have highlighted the importance of
multifactoral explanations. For example, based on a 68-month study of howler monkeys
(Alouatta palliata) and a parasitic bot fly (Alouattamyia baeri), Milton (1996) concluded
that the annual pattern of howler mortality results from a combination of effects
including: age, physical condition, and larval burden of the parasitized individual, which
becomes critical when the population experiences dietary stress (see also Milton et al.
1994). Similarly, Gulland (1992) studied the interactions of Soay sheep and nematode


97
Stuart M.D., L.L. Greenspan, K.E. Glander, and M.R. Clarke. 1990. A coprological
survey of parasites of wild mantled howling monkeys, Alouatta palliata palliata.
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Stuart M.D. and K.B. Strier. 1995. Primates and parasites: a case for a multidisciplinary
approach. International Journal of Primatology 16:577-593.
Stuart M.D., K.B. Strier, and S.M. Pierberg. 1993. A coprological survey of parasites of
wild muriquis, Brachyteles arachnoides, and brown howling monkeys, Alouatta
fusca. Journal of the Helminthological Society of Washington 60:111-115.
Summerville K.S. and T.O. Crist. 2002. Effects of timber harvest on forest Lepidoptera:
community, guild, and species responses. Ecological Applications 12:820-835.
Tabarelli M., W. Mantovani, and C. Peres. 1999. Effects of habitat fragmentation on
plant guild structure in the montane Atlantic forest of southeastern Brazil.
Biological Conservation 91:119-127.
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42
There is good evidence that logging has greatly reduced guenon food availability at
Kibale. First, recall that approximately 50% of all trees in logged forests were destroyed
by felling and incidental damage and that trees harvested were disproportionately primate
food trees (Skorupa 1988; Struhsaker 1997). This reduction in food availability
following logging likely accounts for much of the initial declines seen in guenon and red
colobus populations. Second, even 25 years after logging, tree growth rates and tree
density for all size classes were lower, while seedling mortality was higher in the logged
compared to undisturbed forests (Chapman and Chapman 1997). This suggests that
logged forests are regenerating poorly. So why have red colobus started to recover, while
guenons have not in logged forests? Recall that selective logging facilitates higher
foliage density as a result of greater sunlight availability (Ganzhom 1995). This
translates to greater food availability and food quality (e.g., a predominance of young
leaves) for the folivorous colobines. In addition, the tree species that colonize disturbed
areas (i.e., Celt is durandii and Funtumia latifolia) have leaves with a higher protein-to-
fiber ratio (i.e., higher food quality; Milton 1998), a component of leaves important in
determining colobine abundance (Chapman and Chapman 2002). From 1990 to 2000, the
total basal area of both C. durandii and F. latifolia, major food species for both
colobines, increased substantially in the logged forest (Chapman and Chapman, in press).
During this same period, growth rates for both of these tree species were higher in the
logged compared to the undisturbed forests (Chapman and Chapman, in press).
Concurrently, food resources for the frugivorous guenons have not been recovering.
Multiple indices of fruit production demonstrated lower fruit availability in the logged
compared to undisturbed forests even 25 years after logging (Chapman and Chapman


55
Materials and Methods
Study Site
I surveyed 20 forest fragments that lie within the agricultural landscape from the
western boundary of Kibale National Park to the foothills of the Ruwenzori Mountains in
Uganda (013'-04r N, 3019'-3032') (Onderdonk and Chapman 2000). Mean annual
rainfall in the region is 1749 mm (1990-2001) and mean daily minimum and maximum
temperatures are 14.9C and 20.2C, respectively (1990-2001, Chapman and Chapman
unpublished data). Rainfall is bimodal, with two rainy seasons generally occurring from
March to May and September to November.
Prior to agricultural expansion, mid-elevation, moist, evergreen forest dominated
the region (Naughton-Treves 1997). While the precise timing of isolation of these forest
remnants is not known, local elders describe them as 'ancestral forests', and aerial
photographs from 1959 confirm that most have been isolated from Kibale since at least
that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha, are used by
local citizens to varying degrees, and are surrounded by small-scale agriculture or tea
plantations.
I surveyed compartment K-30, a 282-ha area of undisturbed forest situated within
the largely forested Kibale National Park (746 km2)(Struhsaker 1997). Compartment K-
30 is in close proximity to the forest fragments (< 6.5 km apart), and once belonged to the
same tract of forest, minimizing the probability that differences observed are the result of
inherent variation in forest structure and diversity.
Fecal Sampling and Analysis
From August 1999 to July 2003,1 collected 1,151 fecal samples from primates in
20 forest fragments and the K-30 compartment of Kibale National Park: 951 from red


Table 2-1. Prevalence (%) of gastrointestinal helminth parasite infections in guenons of western Uganda
Parastie Species
Redtail (n = 235)
Blue (n = 35)
Lhoiste (n = 11)
Vervet (n = 12)
Strongyloides fulleborni
7
6
27
42
Oesophagostomum sp.
10
9
9
0
Unidentified Strongyle
0
0
0
42
Trichuris sp.
29
26
36
58
Streptopharagus sp.
18
14
0
17
Enterobius sp.
1
0
0
0
Bertiella sp.
< 1
0
0
0
Dicrocoeliidae sp.
2
3
0
8
Overall
49
37
55
92


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AGREEMENT_INFO ACCOUNT UF PROJECT UFDC
FILES


Rainfall (mm)
31
Figure 3-1. Inter-monthly variation in parasite infection prevalence of colobus monkeys
and rainfall at Kibale National Park, Uganda. A) Red colobus monkeys. B)
Eatem Black-and-white colobus monkeys. (Grey bars represent rainfall.
Black lines represent parasite prevalence).
Prevalence


38
cyst color, shape, contents, and size. Iodine was occasionally used to facilitate protozoan
identification. Measurements were made to the nearest 0.1 micron SD using an ocular
micrometer fitted to a Zeiss compound microscope. Unknown parasites were
photographed for later identification. Coprocultures and necropsies were used to match
parasite eggs to larvae and adult worms for positive identification (MAFF 1979; Greiner
and Courtney 1999). I report data on helminth eggs per gram of feces (EPG) only as an
indication of environmental contamination (i.e., infection risk), as helminth egg
production is highly variable and rarely indicative of actual infection intensity.
Infection Risk Assessment
From January to August 2002,1 conducted a comparative survey to determine an
index of risk of helminth infection to primates inhabiting logged and undisturbed forests.
Canopy vegetation, ground vegetation, and soil plots from logged and unlogged forests
were collected and analyzed to determine the density of infective-stage individuals for the
two parasite species most prevalent in all three primate species, Trichuris sp. (eggs) and
Oespohagostomum sp. (L3 larvae). Twenty-eight 1 m3 vegetation plots were collected at
a height of 12 m from canopy trees used within the previous two hours by red colobus; 14
from logged forest (K-15), and 14 from undisturbed forest (K-30). Access to the canopy
for collection of vegetative plots was facilitated by single rope climbing technique
(Mitchell, 1982; Laman, 1995). An additional 28 1 m3 ground vegetation plots were
collected below all trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches)
were collected within selected ground vegetation plots, 10 from the logged forest and 10
from the unlogged forest. I used a modified sedimentation technique to recover infective-
stage parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using
a modified Baermann method (Sloss et al. 1994). Samples from all plots were examined


Results 73
Discussion 75
7 SUMMARY AND CONCLUSIONS 80
LIST OF REFERENCES 82
BIOGRAPHICAL SKETCH 99
vii


69
parasites and demonstrated that at times of population crashes sheep were emaciated, had
high nematode burdens, and showed signs of protein-energy malnutrition. In the field,
sheep treated with antihelminthics had lower mortality rates, while experimentally
infected sheep with high parasite loads, but fed nutritious diets, showed no sign of
malnutrition. The potential role of parasites and infectious disease in primate population
dynamics in forest fragments remains largely unexplored.
Helminthic and protozoal parasites can impact host survival and reproduction
directly through pathological effects and indirectly by reducing host condition (Chandra
and Newbeme 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop
and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous
abortion, congenital malformations, and death (Chandra and Newbeme 1977;
Despommier et al. 1995). However, less severe infections are more common and may
impair nutrition, travel, feeding, predator escape, and competition for resources or mates;
or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and
Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate
mechanisms, parasites can potentially regulate host populations (Gregory and Hudson
2000; Hochachka and Dhondt 2000).
To improve our capacity to evaluate the conservation value of forest fragments, I
examined how various fragment attributes affect one ecological process, parasite
infection dynamics, and consider how changes in this process may impact host
populations of red colobus (Piliocolobus tephrosceles) inhabiting a series of forest
fragments in western Uganda.


5
3
O
s:
o
es
a.
-
o
-C
£
s
S3
O
4
3
? -
O
*
Undisturbed
Logged
(n = 38)
(n = 561) (n = 127)
(n = 125)
Redtail Guenon Red Colobus Black-and-White Colobus
Figure 4-1. Mean number of parasite species infecting individual redtail guenon (Cercopithecus ascanius), red colobus (Piliocolobus
tephroceles), and black-and-white colobus (Colobus guereza) in undisturbed and logged forest at Kibale National Park,
Uganda


Prevalence and richness of gastrointestinal parasite infections and magnitude of
multiple infections were greater for guenons in logged than in undisturbed forest, but
these parameters did not differ between forest types for either colobine. Infection-risk
was greater for primates in logged compared to undisturbed forest. Prevalence and
richness of gastrointestinal helminth and protozoan parasite infections and frequency of
multiple infections were greater for red colobus in fragmented than in undisturbed forest,
but these parameters did not differ between these areas for black-and-white colobus.
Infection-risk was greater for colobines in fragmented compared to undisturbed forest.
Inter-fragment comparisons examining 10 potential factors demonstrated that an index of
degradation, tree-stump-density, strongly influenced prevalence of strongyle and
rhabditoid nematodes. Infection risk was also higher in the fragment with highest stump-
density compared to the fragment with lowest stump-density. Fragment size and
colobine density were correlated to prevalence for some nematodes, but in multiple
regression analyses with stump-density, these variable did not explain a significant
amount of variance.
These results demonstrate that selective logging and forest fragmentation have the
capacity to affect parasite infection dynamics in some African primate species. These
changes in infection dynamics may play a role in observed primate declines.
xii


6-3 Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus
monkeys (Piliocolobus tephrosceles) and attributes of the forest fragments they
inhabit near Kibale National Park, Uganda
79


Nematoda 23
Cestoda 25
Trematoda 26
Protozoa 26
Effect of Season and Host Sex on Infection Prevalence 27
Discussion 27
4LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN
AFRICAN PRIMATE POPULATIONS 32
Introduction 32
Materials and Methods 35
Study Site 35
Fecal Sampling and Analysis 37
Infection Risk Assessment 38
Statistical Analyses 39
Results 39
Infection Prevalence and Richness 39
Infection Risk 40
Discussion 40
5ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES
IN FOREST FRAGMENTS 53
Introduction 53
Materials and Methods 55
Study Site 55
Fecal Sampling and Analysis 55
Infection Risk Assessment 56
Colobus Surveys 57
Statistical Analyses 57
Results 57
Infection Prevalence and Richness 57
Infection Risk 58
Colobus Population Dynamics 58
Discussion 59
6VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST
FRAGMENT ATTRIBUTES 67
Introduction 67
Materials and Methods 70
Study Site 70
Fecal Sampling and Analysis 70
Infection Risk Assessment 71
Fragment Characteristics 71
vi


34
Despommier et al. 1995). However, less severe infections are more common and may
impair nutrition, travel, feeding, predator escape, and competition for resources or mates;
or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and
Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate
mechanisms, parasites can potentially regulate host populations (Gregory and Hudson
2000; Hochachka and Dhondt 2000).
Selective logging results in changes in forest structure and food availability
(Skorupa 1988; Ganzhom 1995; Chapman and Chapman 1997; Chapman et al. 2000).
Such changes may alter parasite dynamics in wildlife populations. For example,
Ganzhom (1995) demonstrated that selectively logged forests have higher foliage density
than unlogged forests. Higher foliage density translates to greater surface area exposed to
falling feces and possibly an increased probability of contact with infected fecal material
for arboreal animals. In addition, many forest species are stressed following selective
logging due to reduced food availability. Various forms of environmental stress have
been suggested to increase susceptibility to parasitic infection, and stress and disease are
thought to act synergistically to increase morbidity and mortality (Scott 1988; Holmes
1996; Lafferty and Holt 2003). Reductions in animal condition due to food stress have
been documented to increase vulnerability to infection, and result in lower fertility and
higher mortality (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). In
addition, animal body condition and reproductive status are compromised when parasites
inflict substantial energetic costs (Hudson 1986; Moller 1993; Toque 1993; Rigby and
Moret 2000). However, parasites do not necessarily induce negative effects if hosts have
a sufficient energy or nutrient surplus concurrent with infection (Munger and Karasov


23
stored individually in 5.0-mL sterile vials in 10% formalin solution. Preserved samples
were transported to the University of Florida where they were examined for helminth
eggs and larvae and protozoan cysts using concentration by sodium nitrate flotation and
fecal sedimentation (Sloss et al. 1994). Parasites were identified on the basis of egg or
cyst color, shape, contents, and size. Iodine was used to facilitate protozoan
identification. Measurements were made to the nearest 0.1 micron SD using an ocular
micrometer fitted to a compound microscope, and representatives were photographed.
Coprocultures and necropsies (MAFF 1979) were used to match parasite eggs to larvae or
adults for positive identification.
I performed chi-square tests of independence to compare the prevalence of
infections between colobus species and between host age and sex classes for a subset of
red colobus (n = 401). Pearson correlation was used to test relationships between
monthly rainfall and prevalence of parasites infecting red colobus and black-and-white
colobus.
Results
Nematoda
Superfamily Trichuroidea: Trichuris sp. was identified based on egg size and
morphology (barrel-shape, yellow-brown coloration, and bipolar plugs) and verified by
adults obtained by necropsy. Eggs were found in feces of all colobus species, and
measured 57.3 1.0 X 27.0 1.3 pm for red colobus, 58.2 1.6 X 26.9 1.2 pm for
eastern black-and-white colobus, and 58.8 1.2 X 27.2 1.4 pm for Angolan black-and-
white colobus. Prevalence of T. trichiura was higher in Angolan black-and-white
colobus than eastern black-and-white colobus (X2 = 5.28, d.f. = 1, P < 0.025, Table 3-1),
and red colobus (X2 = 32.95, d.f. = 1, P < 0.001, Table 3-1). Prevalence T trichiura was


37
the structure and composition of the forest (Skorupa and Kasenene 1984; Struhsaker
1997). Hence, compartment K-30 serves as a control plot for my comparisons. As a
control, I assume that differences between the undisturbed compartment and the logged
compartment are due only to the effects of logging. This is not ideal as some differences
could be the result of naturally occurring variation in forest structure. However, these
compartments are in close proximity (< 2 km apart), and there are few marked
differences between them in terms of physical characters that influence forest structure.
The study area has been protected from human exploitation since the 1970s, and
the hunting of primates ceased in the region in the early 1960s (Struhsaker 1997;
Chapman et al. 2000). The site's primates have been studied extensively, with over 30
years of primate research and substantial background information on the majority of
primate species present (Struhsaker 1997; Chapman et al. in press). For these reasons, a
number of primate groups are habituated, encounter rate is high, and long-term data are
available on several groups for most primate species.
Fecal Sampling and Analysis
From August 1997 to August 2002,1 collected 1,076 fecal samples from primates
in forest compartments K-15 and K-30; 157 from red-tail guenons, 231 from black-and-
white colobus, and 688 from red colobus. All samples were collected immediately after
defecation to avoid contamination and examined macroscopically for adult nematodes
and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile vials in a
10% neutral formalin solution. Preserved samples were transported to the University of
Florida where they were examined for helminth eggs and larvae and protozoan cysts
using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994;
Greiner and Courtney 1999). Parasites were counted and identified on the basis of egg or


7
(Williams-Linera 1990; Camargo 1993; Malcolm 1994; Laurance et al. 1996). Higher
foliage density has also been demonstrated for selectively logged forests (Ganzhom
1995). Lower canopy height may increase overlap in arboreal pathways among primates
and higher foliage density may increase the surface area exposed to falling feces.
Consequently, these characters may increase the probability of contact with infected fecal
material for primates. However, microclimatic change resulting from disturbance may
negatively influence the lifecycle of a parasite (Stuart et al. 1993). Forest fragments
maintain higher temperature and higher rates of evaporative drying compared to
continuous forest (Kapos 1989; Laurance et al. 1996; Didham and Lawton 1999). Such
abiotic conditions may result in shorter survival time for free-living larvae within fecal
material because of rapid desiccation (Meade 1983).
Forest fragmentation and selective logging are often accompanied by increased
contact between primates and humans. Primates act as reservoirs for human pathogens
and likewise, humans act as reservoirs for diseases to which other primates are
susceptible (Lopez-Neyra 1949; Brown and Neva 1983; Meade 1983; Horii and Usui
1985; Stuart et al. 1990; Wolfe et al. 1998). With increased population densities of
humans and inflated densities of primates in fragmented habitats, the probability of
contact with infectious fecal material and infected hosts increases. Thus, increased
contact with humans may increase infection risk for primates in forest fragments and
selectively logged forests.
In forest fragments, primate densities may be high because of immigration from
cleared areas (Onderdonk and Chapman 2000). Thus, groups there often have more
restricted, overlapping ranges than do groups in continuous forest. Crowding and re-use


46
intermediate hosts, which include coleopterans, orthopterans, ants, and land snails, while
colobines do not intentionally feed on insects and other invertebrates. Consequently, if
intermediate hosts are more common in logged forests or more intermediate hosts are
infected in logged forests, guenons may have a higher encounter probability for parasites
with indirect life cycles. However, infections with these parasite species are rarely
associated with disease, thus, they are likely of minor importance in regards to guenon
declines in logged forests (Table 4-1).
This study suggests that redtail guenons are more susceptible to parasitic infection
than colobines following selective logging at Kibale National Park in Uganda. Logging
in Kibale is known to impact these frugivorous guenon populations more than folivorous
colobine populations, and parasite dynamics appear to play a role in these patterns of
response. Consequently, conservation initiatives for guenons, and potentially a wide-
range of frugivorous species, should focus on the preservation of intact forests. However,
extractive management plans that avoid the removal of preferred food species, maintain
arboreal pathways, and reduce infection risk may allow for selective logging without the
loss of frugivorous populations.
Although many recent studies and reviews have focused on the conservation
implications of anthropozoonotic disease transmission to wildlife (Stuart and Strier 1995;
Wallis and Lee 1999; Nizeyi et al. 2001; Graczyk et al. 2002; Woodford et al. 2002), the
potential impact of anthropogenic habitat disturbance on disease dynamics in wild
populations has received far less attention. This study demonstrates that one such
disturbance, selective logging, has the capacity to alter parasite dynamics for some
species. Knowledge of how particular species are affected by various forms of ecological


CHAPTER 1
INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE
DYNAMICS
Overview
Tropical forests, although covering only 6% of Earth's arable surface, account for
nearly 50% of all known species (National Research Council 1992). Less than 5% of
tropical forests are legally protected (Redford 1992; Oates 1996; Chapman et al. 2000)
and unprotected forests are being degraded at staggering rates (FAO 1999; Chapman and
Peres 2001). Consequently, conservation of many tropical forest species (such as
primates) will depend, at least in part, on the capacity of disturbed areas outside of
reserves to support their populations.
Ninety percent of primate species are restricted to the tropics (Mittermeier and
Cheney 1987), and more than half of primate species are threatened by extinction
(Chapman and Peres 2001). Thus, primates represent an ideal taxa for studying the
effects of human disturbance in tropical forests. Although human disturbance is known
to negatively impact primate populations, little is known about the mechanisms
responsible for such effects. One such mechanism may be infection dynamics.
Emerging tropical diseases (such as AIDS and Ebola) have raised global awareness
of the strong linkage between biodiversity conservation and the health of animal and
human populations (Meffe 1999; Daszak et al. 2000, 2001). To effectively understand
the dynamics of emerging diseases, we must evaluate the interplay among alteration and
fragmentation of tropical forests, wildlife-human disease linkages, and the ecology of
1


28
noteworthy. Unlike red colobus, eastern black-and-white colobus are known to descend
into swampy areas to feed on aquatic vegetation (Oates 1978) where incidental ingestion
of intermediate host or encysted trematodes is likely. Also, eastern black-and-white
colobus are known to come to the group to eat soil and charcoal, much more frequently
than red colobus (Gillespie pers. obs.). This may explain the higher prevalence of the
dicrocoeliid liver fluke in eastern black-and-white colobus than red colobus.
Seasonal patterns of infection were not readily apparent for any of the parasite
species infecting red colobus or eastern black-and-white colobus. This result is
unexpected, as previous studies of parasite infections from tropical forest frugivorous
monkeys and apes have documented an increase in prevalence during the rainy season
(Lophocebus albigena Freeland 1977; Pan troglodytes Huffman et al. 1997). It is
difficult to determine why seasonal differences were not seen in these folivores.
However, variation in infection prevalence was evident over the year, warranting future
investigation of the mechanism behind these differences (Figure 3-1).
Prevalence of S. fulleborni was higher in adult male compared to adult female red
colobus. Perhaps this reflects energy and nutrient stress associated with maintaining
social dominance (Hausfater and Watson 1976), which may result in an increased
susceptibility to infection (Gulland 1992; Milton 1996). However, if this is the case, it is
not clear why infection prevalence is not higher for other parasite species in males
compared to females.
Freeland (1977) provided a survey of the protozoan parasites of primate species in
Kibale National Park that failed to document the presence of any protozoan in colobus
feces based on examination of a small number of samples for red colobus (n = 5) and


13
and 57.9 1.4 X 26.7 1.6 pm for vervets. Prevalence of infection with Trichuris sp.
did not differ between redtail guenons (30%) and blue monkeys (26%) (P > 0.05, Table
2-1).
Strongyloidea: Oesophagostomum sp. was identified on the basis of egg size and
morphology (elliptical, unlarvated) and cultured larvae. Eggs were found in feces of all
guenon species except vervets, and measured 69.1 1.8 X 42.4 2.0 pm for redtail
guenons, 70.5 2.0 X 41.3 1.7 pm for blue monkeys, and 73.1 1.2 X 43.0 1.4 pm
for l'hoesti monkeys. Prevalence of Oesophagostomum sp. did not differ (P > 0.05)
between redtail guenons (10%) and blue monkeys (9%) (Table 2-1). Unidentified
strongyle eggs were found in vervet feces (42%) and measured 72-52 X 42-35 pm.
These strongyles may represent Nectator sp., Ancylostoma sp., and/or Oesophagostomum
sp.; however, coprocultures were not performed, limiting our ability to identify these
parasites.
Rhabditoidea: Strongyloides fulleborni was identified based on egg size and
morphology (oval, thin-shelled, colorless, larvated) and verified by cultured rhabditiform
larvae. Eggs were found in feces of all guenon species, and measured 50.2 2.3 X 33.7
4.1 pm for redtail guenons, 43.7 5.0 X 35.4 3.1 pm for blue monkeys, 46.5 3.4 X
34.6 2.3 pm for l'hoesti monkeys, and 47.1 3.7 X 34.4 2.6 pm for vervets.
Prevalence of infection with S. fulleborni did not differ between redtail guenons (7%) and
blue monkeys (6%) (P > 0.05, Table 2-1).
Oxyuroidea: Eggs that appear to be Enterobius sp. based on egg size and
morphology were found in 2 redtail guenon samples (Table 2-1), and measured 64-66 X
36-37 pm (n = 2). This parasite is more reliably diagnosed by examination of peri-anal


CHAPTER 7
SUMMARY AND CONCLUSIONS
Emerging infectious diseases have raised global awareness of the potential impact
that ecological change can have on biodiversity conservation and wildlife and human
health. This study improves our understanding of this interplay by examining the effects
of logging and forest fragmentation on parasite dynamics in an African primate
community. The most important contributions of this study are as follows.
1. This study provided the first reports of gastrointestinal helminth parasites from wild
populations of redtail guenons, l'hoesti monkeys, red colobus, and black-and-white
colobus and the first report of gastrointestinal helminth parasites from blue and
vervet monkeys from Uganda. This baseline data on the patterns of parasitic
infection in wild monkeys provides a first step toward an index of population health
and disease risk assessment for conservation and management plans of threatened
and endangered African primate populations.
2. This study demonstrated that selective logging was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus, black-and-white colobus, and redtail guenons. Despite
this higher infection risk for all species, only redtail guenons manifested higher
prevalence and richness of gastrointestinal parasite infections and greater
magnitude multiple-infections in logged compared to undisturbed forests. These
results suggest that redtail guenons are more susceptible to parasitic infection
following selective logging than colobines.
3. This study demonstrated that forest fragmentation was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus and black-and-white colobus. Despite this higher infection
risk for both species, only red colobus manifested higher prevalence and richness of
gastrointestinal parasite infections and greater magnitude muliple-infections in
fragmented compared to undisturbed forests. These results suggest that red colobus
are more susceptible to parasitic infection following forest fragmentation than
black-and-white colobus.
4. This study demonstrated that humans, and potentially livestock, are exposing
colobus in forest fragments to novel pathogens. Four species infecting red colobus
(Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified
80


BIOGRAPHICAL SKETCH
Thomas R. Gillespie was bom in Rockford, IL, on 16 September 1974. Gillespie
received his B.Sc. in Ecology, Ethology, and Evolution in May 1996 from the University
of Illinois, Urbana-Champaign. After completing his undergraduate studies, he worked
with the Universidad Nacional de la Amazonia Peruana and Dr. Carl Bouton of the
University of Illinois to develop and establish a semi-autonomous environmental
education program for the school system of Iquitos, Peru. He joined the department of
zoology at the University of Florida in 1997 and, working with Dr. Colin A. Chapman,
was awarded his M.Sc. in 2000. For the past seven years, he has been working with
African, European, and North American colleagues on a long-term investigation of the
effects of anthropogenic disturbance (i.e., selective logging and forest fragmentation) on
the ecology and behavior of wildlife in Kibale National Park and surrounding areas in
Uganda. Since 1999, parasite and disease dynamics have become central to his role in
these collaborations. Gillespie is a STAR fellow of the United States Environmental
Protection Agency, a member of the IUCN Veterinary Specialist Groups Great Ape
Health Monitoring Unit (GAHMU), serves on a national advisory committee to Amnesty
International on topics at the nexus of conservation and human rights, and assists the
BBC Natural History Unit as a biological consultant.
99


LIST OF TABLES
Table
page
2-1 Prevalence (%) of gastrointestinal helminth parasite infections in guenons of
western Uganda 19
3-1 Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys
of Uganda 30
4-1 Mode of infection, morbidity, and mortality associated with gastrointestinal
parasites infecting redtail guenon (Cercopithecus ascanius), red colobus
(Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda 48
4-2 Prevalence (%) of gastrointestinal parasite infections in redtail guenons
(Cercopithecus ascanius) from logged and undisturbed forests in Kibale National
Park, Uganda 49
4-3 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from logged and undisturbed forests in Kibale National Park, Uganda50
4-4 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from logged and undisturbed forests in Kibale National Park,
Uganda 51
5-1 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from forest fragments and undisturbed forests in Kibale National Park,
Uganda 63
5-2 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from forest fragments and undisturbed forests in Kibale
National Park, Uganda 64
6-1 Physical and biological attributes of forest fragments with red colobus
(Piliocolobus tephroceles) populations near Kibale National Park, Uganda 77
6-2 Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus
monkeys (Piliocolobus tephroceles) in forest fragments near Kibale National Park,
Uganda 78
viii


24
higher in eastern black-and-white colobus than red colobus (X2 = 249.94, d.f. = 1, P <
0.001, Table 3-1).
Superfamily Strongyloidea: Oesophagostomum sp. was identified on the basis of
egg size and morphology (elliptical and unlarvated) and verified by cultured larvae and
adults obtained by necropsy. Eggs were found in feces of all colobus species except
Angolan black-and-white colobus, and measured 70.0 1.4 X 41.8 1.6 pm for red
colobus and 70.2 1.8 X 41.6 1.6 pm for eastern black-and-white colobus. Prevalence
of Oesophagostomum sp. was higher in eastern black-and-white colobus than in red
colobus (X2 11.40, d.f. = 1, P < 0.001, Table 3-1).
Unidentified strongyle eggs were found in feces of all colobus species and
measured 59.6 5.6 X 38.2 4.1 pm for red colobus, 63.7 4.8 X 40.1 4.5 pm for
eastern black-and-white colobus, and 68.4 2.0 X 40.3 2.3 pm for Angolan black-and-
white colobus. These strongyles may represent Necator sp., Ancylostoma sp., and/or
Oesophagostomum sp.; however coprocultures were not performed, limiting our ability to
identify these parasites to genus level. Prevalence of unidentified strongyles was higher
for Angolan black-and-white colobus than for either red colobus (X2 = 9.18, d.f. = 1, P <
0.005, Table 3-1) or eastern black-and-white (X2 = 11.87, d.f. = 1, P < 0.001, Table 3-1).
Superfamily Rhabditoidea: Strongyloides fulleborni was identified based on egg
size and morphology (oval, thin-shelled, colorless, and larvated) and verified by cultured
rhabditiform larvae. Eggs were found in feces of all colobus species, and measured 45.7
1.7 X 34.8 2.0 pm for red colobus, 46.7 2.2 X 35.2 2.2 pm for eastern black-and-
white colobus, and 47.0 1.8 X 35.4 2.0 pm for Angolan black-and-white colobus.
Prevalence of S. fulleborni did not differ among colobus species (P > 0.1, Table 3-1).


This dissertation was submitted to the Graduate Faculty of the Department of
Zoology in the College of Liberal Arts and Sciences and to the Graduate School and was
accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy.
August 2004
Dean, Graduate School


CHAPTER 6
VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST
FRAGMENT ATTRIBUTES
Introduction
For fragmented forests to have conservation value, they must retain ecological
integrity sufficiently to maintain species and biological processes over the long-term.
Studies have highlighted the importance of physical attributes such as fragment size,
shape, and isolation (Laurance and Bierregaard 1997); and biological attributes such as
predator, prey, and tree density and diversity on ecological processes and species survival
probabilities (Crooks and Soule 1999; Terborgh et al. 2001; Laurance et al. 2002).
However, despite the large scope of this research, our capacity to predict how ecological
processes will be altered and which taxonomic or functional groups will be most affected
by fragmentation is still poor.
Such difficulties are well illustrated by primates inhabiting forest fragments. No
clear generalizations emerge as to what types of primates are most susceptible to
fragmentation, nor what types of fragments are most likely to support primates, despite a
growing body of research (Tutin et al. 1997; Onderdonk and Chapman 2000; Marsh
2003). Our inability to evaluate the potential of forest fragments for primate conservation
appears to be driven by several factors. First, most previous work has been conducted in
fragments protected from human use (Lovejoy et al. 1996; Tutin et al. 1997; Gilbert
2003); however, typically fragments are not protected and are characterized by open
access by private citizens who depend on them for fuelwood, medicinis, or bushmeat
67


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Ct I.M. and R. Poulin. 1995. Parasitism and group size in social animals: a meta
analysis. Behavioural Ecology 6:159-165.
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chimpanzee. Receuil de medicine Veterinaire de l'Ecole d'Alfort 151:13-18.
Crompton D.W.T. 1991. Nutritional interactions between hosts and parasites. Pages 228-
257. In C.A. Toft, A. Aeschlimann, and L. Bolis (eds.). Parasite-host associations:
coexistence or conflict. Oxford University Press, Oxford.
Crooks K. R. and M.E. Soule. 1999. Mesopredator release and avifaunal extinctions in a
fragmented system. Nature 400:563-566.
Daszak P., A.A. Cunningham, and A.D. Hyatt. 2000. Wildlife ecology emerging
infectious diseases of wildlife- threats to biodiversity and human health. Science
287:443-449.
Daszak P., A.A. Cunningham, and A.D. Hyatt. 2001. Anthropogenic environmental
change and the emergence of infectious diseases in wildlife. Acta Tropica 78:103-
116.
Davies C.R., J.M. Ayres, C. Dye, and L.M. Deane. 1991. Malaria infection rate of
Amazonian primates increases with body weight and group size. Functional
Ecology 5:655-662.
Deem S.L., W.B. Karesh, and W. Weisman. 2001. Putting theory into practice: wildlife
health and conservation. Conservation Biology. 15:1224-1233.
DePaoli A. and D.O. Johnsen. 1978. Fatal strongyloidiasis in gibbons (Hylobates lar).
Veterinary Pathology 15:31-39.
Despommier D.D., R.W. Gwazda, and P.J. Hotez. 1995. Parasitic Diseases. Springer-
Verlag, New York.
Didham R.K. and J.H. Lawton. 1999. Edge structure determines the magnitude of
changes in microclimate and vegetation structure in tropical forest fragments.
Biotropica 31: 17-30.
Dobson A.P. 1995. Biodiversity and human health. Trends in Ecology and Evolution
10:390-391.
Dobson A.P. and P.J. Hudson. 1992. Regulation and stability of a free-living host-
parasite system: Trichostrongylus tenuis in red grouse: 2 population models.
Journal of Animal Ecology 61:487-498.
Dobson A.P. and R.M. May. 1986. Disease and conservation. Pp. 345-365, in M.E.
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McClure H. and N. Guilloud. 1971. Comparative Pathology of the Chimpanzee. Karger,
Basel.
McGrew W.C., C.E.G. Tutin, D.A. Collins, and S.K. File. 1989. Intestinal parasites of
sympatric Pan troglodytes and Papio spp. at two sites: Gombe (Tanzania) and Mt.
Assirik (Senegal). American Journal of Primatology 17:147-155.
McGrew W.C., C.E.G. Tutin, and S.K. File. 1989. Intestinal parasites of two species
offfee-living monkeys in far western Africa, Cercopithecus (aethiops) sabaeus
andErythrocebus patas patas. African Journal of Ecology 27: 261-262.
Mead B.J. 1983. Host-parasite dynamics among Amboseli baboons (Papio
cynocephalus). Ph.D. Dissertation. Virginia Polytechnic Institute and State
University, VA.
Meffe G. 1999. Conservation Medicine. Conservation Biology 13:953-954.
Mesquita R., P. Delamonica, and W.F. Laurance. 1999. Effects of surrounding
vegetation on edge-related tree mortality in Amazonian forest fragments.
Biological Conservation 91:129-134.
Mihook S., B.N. Turner, and S.L. Iverson. 1985. The characterization of vole population
dynamics. Ecological Monographs 55:399-420.
Milton K. 1982. Dietary quality and demographic regulation in a howler monkey
population. Pp. 273-289, in E.G. Leigh Jr, A.S. Rand, and D.M. Windsor, eds. The
Ecology of a Tropical Forest. Smithsonian Institution Press, Washington, D.C.
Milton K. 1996. Effects of hot fly (Alouattamyia baeri) parasitism on a free-ranging
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growth of large trees in a Panamanian lowland forest. Journal of Ecology 82:79-
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89
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Evolution 11:185-194.


CHAPTER 3
GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF UGANDA
Introduction
Colobinae is a large subfamily of leaf-eating, old-world monkeys represented in
Africa by two genera, Colobus and Piliocolobus (Grubb et al. 2002). These folivorous
monkeys live in groups of highly variable size (5-300 individuals) and often form mixed-
species associations with other primates (Struhsaker 1981; Oates 1994; Chapman and
Chapman 2000). Colobus species are forest-dependent, and consequently, acutely
threatened by human activities that reduce forest cover. More than two-thirds of Sub-
Saharan Africas original forest cover has been lost due to anthropogenic disturbance
(World Resources Institute 1998), and forest cover continues to decline at a rate of 0.7%
annually (FAO 1999). Due largely to this habitat loss, 50% of African colobine species
are endangered and an additional 20% are rare (Grubb et al. 2002).
Although parasite infections are common in nature and low-intensity infections are
often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic
change may result in a loss of stability associated with altered transmission rates, host
range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline
data on patterns of parasitic infections in wild colobine populations are critical to provide
an index of population health and to begin to assess and manage disease risks.
Although many studies have documented the gastrointestinal parasites of wild
populations of African apes (Huffman et al. 1997; Nizeyi et al. 1999; Graczyk et al.,
1999; Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et
21


22
al. 1989; Mller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other
African primate taxa remain poorly known. This study identifies and quantifies the
prevalence of gastrointestinal helminth and protozoan parasites for the three colobus
species of Uganda: the endangered red colobus (Piliocolobus tephroceles), the eastern
black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus
(Colobus angolensis). Where data are sufficient, I also examine the effect of season and
host sex on parasite prevalence.
Materials and Methods
From August 1997 to July 2003,1 collected 2,103 fecal samples: 1,608 from red
colobus, 476 from eastern black-and-white colobus, and 19 from Angolan black-and-
white colobus. Red colobus and eastern black-and-white colobus samples were collected
in 21 forest fragments in Western Uganda, and at Kanyawara, a 1,034 ha area
characterized by logged and unlogged forest within Kibale National Park (766 km2;
013'-04r N, 30o19'-3032' E; Struhsaker 1997). Mean annual rainfall (1990-2001) is
1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged
14.9C and 20.2C, respectively, from 1990 to 2001. Angolan black-and-white colobus
samples were collected from three forest fragments adjacent to Lake Nabugabo in
Southeastern Uganda (0o20-025' S, 3150'-3156 E). Annual rainfall ranges from 520
to 1,970 mm (Efitre et al. 2001) and daily temperature minima and maxima average
15.2C and 27.2C, respectively (Meteorology Department, Masaka, Uganda). All sites
experience a bimodal pattern of seasonal rainfall, with peaks occurring in March-May
and August-November (Figure 3-1).
Samples were collected immediately after defecation to avoid contamination and
examined macroscopically for adult nematodes and tapeworm proglottids. Samples were


56
colobus and 200 from black-and-white colobus. All samples were collected immediately
after defecation to avoid contamination and examined macroscopically for adult
nematodes and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile
vials in a 10% formalin solution. Preserved samples were transported to the University
of Florida where they were examined for helminth eggs and larvae and protozoan cysts
using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al.
1994). Parasites were counted and identified on the basis of egg or cyst color, shape,
contents, and size. Iodine was occasionally used to facilitate protozoan identification.
Measurements were made to the nearest 0.1 micron SD using an ocular micrometer
fitted to a compound microscope. Unknown parasites were photographed for later
identification. Coprocultures and necropsies were used to match parasite eggs to larvae
and adult worms for positive identification (MAFF 1979).
Infection Risk Assessment
As an index of infection risk, infective-stage parasite densities were determined for
canopy vegetation, ground vegetation, and soil plots from fragmented and undisturbed
forest. From January to August 2002,1 collected twenty-nine 1 m3 vegetation plots at a
height of 12 m from canopy trees used within the previous 2 hr by red colobus; 15 from
forest fragments and 14 from undisturbed forest. Canopy access for plot collection was
facilitated by single rope climbing technique (Mitchell 1982). An additional 29 1 m3
ground vegetation plots were collected below all trees sampled for canopy plots. Soil
plots (0.05 m3 surface scratches) were collected within randomly selected ground
vegetation plots, 10 from forest fragments and 10 from undisturbed forest. I used a
modified sedimentation technique to recover infective-stage parasites from vegetative
plots (Sloss et al. 1994). Soil plots were examined using a modified Baermann method


54
stressors associated with forest fragmentation, such as reduced food availability and
diversity, density-dependent factors, and more frequent interactions with humans may
reduce immunity and elevate susceptibility to infection (Murray et al. 1998; Lafferty and
Holt 2003). Reduced habitat area following forest fragmentation may result in restricted
ranging and crowding (McCallum and Dobson 2002; Lafferty and Holt 2003), increasing
habitat overlap among conspecifics, thus predisposing individuals to a higher probability
of pathogen contact (Freeland 1977; Altizer 2003). Landscape characteristics of
fragment boundaries influence the frequency and nature of contact among wildlife,
human, and livestock populations, increasing the potential for epizootic and
anthropozoonotic pathogen transmission (Lafferty and Gerber 2002; McCallum and
Dobson 2002).
To improve our understanding of how fragmentation alters infection dynamics, I
quantified gastrointestinal parasites of the endangered red colobus (Piliocolobus
tephroceles) and black-and-white colobus (Colobus guereza) populations in western
Uganda between August 1999 and July 2003. I compare the prevalence, diversity,
number of gastrointestinal parasite species infecting individuals, and relative infection
risk for primates between forest fragments and undisturbed forests within Kibale National
Park. Concurrent censuses of colobus populations allowed us to examine infection
dynamics in relation to host-population dynamics. Our investigation proposes a novel
mechanism for vertebrate declines in forest fragments and addresses implications of these
findings for conservation strategies.


8
of restricted areas may increase the probability of a primate coming into contact with an
infected individual or areas contaminated with infectious fecal material. For example,
chimpanzees (Pan troglodytes) and howling monkeys (Alouatta palliata and A.
seniculus) demonstrate higher prevalence of parasite infections in groups with restricted
ranges or in groups at higher population density (McGrew et al. 1989; Stuart et al. 1990;
Gilbert 1994). Gilbert (1994) also demonstrated that prevalence of endoparasitic
infection was positively correlated with the density of sympatric primate species. Thus,
crowding resulting from forest fragmentation may increase transmission of infectious
parasites among primates.
If there is a reduction of food availability associated with forest fragmentation or
selective logging, this may result in decreased animal condition. Reductions in animal
condition due to food stress can increase vulnerability to disease or parasites, resulting in
population declines (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). Thus,
it appears likely that human disturbance, such as forest fragmentation and high-intensity,
selective logging may alter the risk of parasite infection for primates.
Rationale
My objective was to determine the consequences of various forms of human
disturbance (including selective logging and forest fragmentation) on primate-parasite
dynamics. To meet this objective, I intensively surveyed the primate community of
Kibale National Park and surrounding areas to determine prevalence and diversity of
gastrointestinal parasites. Chapter 2 presents the findings of these surveys for the guenon
species. Chapter 3 presents the findings of these surveys for the colobine species. Next,
I compared infection dynamics for red colobus, black-and-white colobus, and redtail
guenons between selectively logged forest and undisturbed forest. Details of this aspect


5
Primate-Parasite Dynamics
Gastrointestinal parasites infecting mammals are commonly transmitted through
contact with the free-living stages, ova, or larvae. This may involve contact with
contaminated food, water, fecal material, or soil (with vertebrate or invertebrate vectors),
or may involve direct contact with infected individuals (Brown and Neva 1983).
Parasites impact host survival and reproduction directly through pathological effects, and
indirectly by reducing host condition (Chandra and Newbeme 1977; Hart 1988, 1990,
1992; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Despommier et al.
1995; Coop and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage,
spontaneous abortion, congenital malformations, and death (Chandra and Newbeme
1977; Despommier et al. 1995). Less severe infections may impair nutrition; may
increase energy expenditure; or may impair travel, feeding, escape from predators, and
competition for resources or mates (resulting in mortality or lower fitness) (Boyce 1990;
Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996; Hart 1988, 1990,
1992). Through these proximate mechanisms, parasites can ultimately regulate host
populations (Gregory and Hudson 2000; Hochachka and Dhondt 2000) or cause short
term reductions in population size (Collias and Southwick 1952; Work et al. 1957).
Few studies have investigated the effects of parasite infections on wild primate
populations. However, evidence suggests that parasite infections can lead to primate
mortality. For example, Ohsawa (1979) and Dunbar (1980) demonstrated that larval
cestode infections contributed to high mortality rates for immature and older gelada
baboons (Theropithecus gelada). Several studies have demonstrated endoparasitic,
ectoparasitic, and viral epidemics in great ape populations in areas near human settlement
(Ashford et al. 1990; Hastings et al 1991; Kortlandt 1996; Meader et al. 1997; Pussey


94
Nizeyi J.B., R. Mwebe, A. Nanteza, M.R. Cranfield, G.R.N.N. Kalema, and T.K.
Graczyk. 2001. Crytosporidium sp. and Giardia sp. infections in mountain gorillas
(Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda.
Journal of Parasitology 85:1084-1088.
Norval R.A.I., B.D. Perry, and A.S. Young. 1992. Pages 223-234 and 285-290 in The
epidemiology of theileriosis in Africa. Academic Press, London.
Nowak M.A. and R.A. May. 1994. Superinfection and the evolution of parasite virulence.
Proceedings of the Royal Society of London 255:81-89.
Oates J. F. 1974. Ph.D. dissertation. University of London, London.
Oates J.F. 1978. Water, plant and soil consumption by guereza monkeys (Colobus-
guereza): relationship with minerals and toxins in the diet. Biotropica 10:241-253.
Oates J.F. 1994. African primates in 1992: conservation issues and options. American
Journal of Primatology 34:61-71.
Oates J.F. 1996. Habitat alteration, hunting and the conservation of folivorous primates in
African forests. Australian Journal of Ecology 21:1-9.
Obendorf D. and D.M. Spratt. 1995. Wildlife disease and its relevance to conservation
biology and biodiversity. Australasian Biotechnology 5:217-219.
Ohsawa H. 1979. The local gelada population and environment of the Gich area. Pp. 4-
45, in M. Kawai, ed. Ecological and Sociological Studies of Gelada Baboons,
Contributions to Primatology, Volume 16. Karger, Basel.
Onderdonk D.A. and C.A. Chapman. 2000. Coping with forest fragmentation: the
primates of Kibale National Park, Uganda. International Journal of Primatology
21:587-611.
Osmaton H.A. 1959. Working plan for the Kibale and Itwara forests. Uganda Forest
Department, Entebbe, Uganda.
Ott-Joslin J.E. 1993. Zoonotic diseases of nonhuman primates. Pp. 358-373, in M.
Fowler, ed. Zoo and Wildlife Medicine Current Therapy. W.B. Saunders and
Company, Philadelphia, PA.
Packer C., R.D. Holt, P.J. Hudson, K.D. Lafferty, and A.P. Dobson. 2003. Keeping the
herds healthy and alert: implications of predator control for infectious disease.
Ecology Letters 6:1-6.
Pampiglione S. and M.L. Ricciardi. 1972. Geographic distribution of Stongyloides
fullebomi in humans in tropical Africa. Parassitologia 14:329-338.


96
Ruvolo M. 1988. Genetic evolution in the African guenons. Pp. 217-139, in A. Gautier-
Hion, F. Bourliere, and J.P. Gautier, eds. A Primate Radiation: Evolutionary
Biology of the African Guenons. Cambridge University Press, Cambridge.
Scott M.E. 1988. The impact of infection and disease on animal populations: implications
for conservation biology. Conservation Biology 2:40-56.
Skorupa J.P. 1988. The effect of selective timber harvesting on rain-forest primates in
Kibale Forest, Uganda. Ph.D. Dissertation, University of California, Davis, CA.
Skorupa J.P. and J. M. Kasenene. 1984. Tropical forest management: can rates of natural
treefalls help guide us? Oryx 18:96-101.
Sloss M.W., R.L. Kemp, and A.M. Zajac. 1994. Veterinary Clinical Parasitology (6th
edition). Iowa State University Press, Ames, IA.
Solomons N.W. and M.E. Scott. 1994. Nutrition status of host populations influences
parasitic infections. Pages 101-114. in M.E. Scott and G. Smith (eds.). Parasitic and
infectious diseases. Academic Press, New York, New York.
Soulsby E. 1982. Helminths, arthropods and protozoa of domesticated animals. 7th
Edition, Balliere Tindall, London.
Smith C.C. 1977 Feeding behaviour and social behavior in howling monkeys. Pp. 97-
126, in T.H. Clutton-Brock, ed. Primate Ecology. Academic Press, London.
Spalding M.G. and D.J. Forrester. 1993. Disease monitoring of free-ranging and released
wildlife. Journal of Zoo and Wildlife Medicine 24:271-280.
Stien A., R.J. Irvine, E. Ropstad, O. Halvorson, R. Langvatn, and S.D. Albon. 2002. The
impact of gastrointestinal nematodes on wild reindeer: experimental and cross-
sectional studies. Journal of Animal Ecology. 71:937-945.
Struhsaker T.T. 1975. The Red Colobus Monkey. University of Chicago Press, Chicago.
Struhsaker T.T. 1976. A further decline in numbers of Amboseli vervet monkeys.
Biotropica 8:211-214.
Struhsaker, T.T. 1981. Polyspecific associations among tropical rain-forest primates.
Zeitschrift Fur Tierpsychologie 57:268-304.
Struhsaker T.T. 1997. Ecology of an African Rain Forest: Logging in Kibale and the
Conflict Between Conservation and Exploitation. University Press of Florida,
Gainesville, FL.
Struhsaker T.T. and M. Leaky. 1990. Prey selectivity by crowned hawk eagles on
monkeys in Kibale Forest, Uganda. Behavioral Ecology and Sociobiology 26: 435-
443.


CHAPTER 5
ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES IN
FOREST FRAGMENTS
Introduction
Forest fragmentation reduces overall species diversity and alters species abundance
(Laurance and Bierregaard 1997; Laurance 1999); modifying biological processes such as
predation, competition, and infection dynamics (Crooks and Soule 1999; Terborgh et al.
2001; LoGuidice et al. 2003). To date, empirical evidence has been lacking to test the
relative importance of these factors in explaining the complex relationship between
wildlife declines and fragmentation-induced ecological change. I present support for a
previously unrecognized mechanism for vertebrate declines following forest
fragmentation, altered infection dynamics.
Parasite infections are common in nature and low-intensity infections are often
asymptomatic. Stability is common, resulting in coexistence of parasite, vector, and host
such that clinical disease is unusual (Anderson and May 1979; May and Anderson 1979).
However, anthropogenic change may result in a loss of stability associated with altered
vector dynamics, transmission rates, parasite host range, and parasite virulence (May
1988; Daszak et al. 2000; Patz et al. 2000). Resultant changes in host susceptibility and
infection risk may result in elevated morbidity and mortality, and ultimately, population
declines.
Forest fragmentation results in a suite of alterations that may increase susceptibility
to infection and infection risk in resident populations (Figure 5-1). Environmental
53


Table 6-2. Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus monkeys (Piliocolobus tephroceles) in
forest fragments near Kibale National Park, Uganda
Fragment
N
Oesophagostomum sp.
Unidentified Strongyle
Strongyloides fulleborni
Strongyloides stercoralis
Collective
Bugembe
31
3
16
6
0
25
CK
66
2
2
0
0
4
Kifuruka
53
2
0
4
0
6
Kiko 1
45
5
9
11
9
34
Kiko 2
40
7
0
9
0
16
Kiko 3
25
24
28
16
12
68
Kiko 4
44
3
9
5
0
17
Nkuruba
179
< 1
0
0
0
< 1
Rutoma
53
0
6
0
0
6
Average
N.A.
5
8
6
2
20


Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS
By
Thomas R. Gillespie
August 2004
Chair: Colin A. Chapman
Major Department: Zoology
Emerging infectious diseases have raised global awareness of the impact ecological
change can have on biodiversity conservation and wildlife and human health. This study
improves our understanding of this interplay by examining effects of logging and forest
fragmentation on parasite dynamics in an African primate community. From August
1997 to July 2003, 2,017 fecal samples were collected to compare gastrointestinal
parasite infections of red colobus (Piliocolobus tephroceles), black-and-white colobus
(Colobus guereza), and redtail guenon (Cercopithecus ascanius) populations from logged
(all), fragmented (only colobines), and undisturbed forests (all) at Kibale National Park,
Uganda. Dynamics of red colobus infection with strongyle and rhabditoid nematodes
were examined in relation to forest fragment attributes. Helminth eggs, larvae, and
protozoan cysts were identified using sodium-nitrate flotation and fecal sedimentation.
Coprocultures and necropsies facilitated identification. Infection-risk was quantified by
modified sedimentation technique, comparing densities of infective-stage parasites from
canopy and ground vegetation plots in logged, fragmented, and undisturbed forest.
xi


57
(Sloss et al. 1994). Samples were examined by dissecting and compound scope, and
infective-stage individuals of the two most prevalent parasite species, Trichuris trichuria
(eggs) and Oespohagostomum stephanostomum (L3 larvae) were counted.
Colobus Surveys
Red colobus and black-and-white colobus populations in forest fragments were
censused from May to August 2000 and recensused May to August 2003. The total
number of colobus in each fragment was counted over 1 to 4 days. Our repeated
censuses of red colobus and black-and-white colobus over the past three decades within
the K-30 compartment of Kibale National Park provide comparable data for these
colobus populations (Chapman et al. 2000).
Statistical Analyses
I employed chi-square tests of independence to compare prevalence between
fragment and undisturbed forest samples for overall and specific infections. Independent
sample t-tests were performed to compare mean number of parasite species infecting
individual primates and density of infective-form parasites in plots between fragmented
and undisturbed forest.
Results
Infection Prevalence and Richness
The prevalence of infection with Trichuris sp., Oespohagostomum sp., Entamoeba
coli, and Entamoeba histolytica was higher for red colobus from forest fragments
compared to red colobus from undisturbed forest, but prevalence did not differ for
Strongyloides fulleborni or Colobenterobius sp. (Table 5-1). Only red colobus from
forest fragments were infected with Strongyloides stercoralis, Ascaris sp., Bertiella sp.,
Giardia lamblia, and unknown strongyles (Table 5-1). There were no species of parasite


35
1989; Gulland 1992; Milton 1996). This suggests that the outcome of host-parasite
associations may be contingent on host nutritional status as well as severity of infection.
Emerging infectious diseases have raised global awareness of the potential impact
ecological change can have on biodiversity conservation and wildlife and human health
(Meffe 1999; Daszak et al. 2000; Patz et al. 2000; Deem et al. 2001; Lafferty and Gerber
2002). To better develop strategies to deal with established and changing patterns of
disease, we must understand the interplay among alteration and fragmentation of
ecosystems, wildlife-human disease linkages, and the ecology of novel diseases. This
study aims to improve our understanding of this interplay by examining the effects of
selective logging on parasite dynamics in three primate species, the redtail guenon
(Cercopithecus ascanius), the red colobus (Piliocolobus tephroceles), and the black-and-
white colobus (Colobus guereza) in Kibale National Park, Uganda. I compare the
prevalence, diversity, and mean number of gastrointestinal parasite species infecting
individuals, and the relative infection risk between primates from logged and undisturbed
forests. My investigation proposes explanations for similarities and differences in
parasite dynamics between logged and undisturbed forests and addresses the implications
of these findings to conservation and management strategies.
Materials and Methods
Study Site
Kibale National Park (766 km2) is located in western Uganda (lat 0 13'-041' N,
long 3019'-3032' E ) near the base of the Ruwenzori Mountains (Struhsaker 1997).
Tall, closed-canopy forest accounts for 57% of the park. The remainder forms a mosaic
of swamp (4%), grasslands (15%), pine plantations (1%), and colonizing forest (19%)
(Chapman and Lambert 2000). The study site, Kanyawara, is located at the northern end


90
Lack D. 1954. The Natural Regulation of Animal Numbers. Oxford University Press,
Oxford.
Lafferty K.D. and L.R. Gerber. 2002. Good medicine for conservation biology: the
intersection of epidemiology and conservation theory. Conservation Biology
16:593-604.
Lafferty K.D. and R.D. Holt. 2003. How should environmental stress affect the
population dynamics of disease? Ecology Letters 6:654-664.
Laman T.G. 1995. Safety recommendations for climbing rain forest trees with single
rope technique Biotropica 27:406-409.
Landsoud-Soukate L, C.E.G. Tutin, and M. Fernandez. 1995. Intestinal parasites of
sympatric gorillas and chimpanzees in the Lope Reserve, Gabon. Annals of
Tropical Medicine and Parasitology 89:73-79.
Laurance W.F. 1999. Ecology and management of fragmented tropical landscapes:
introduction and synthesis. Biological Conservation 91:109-117.
Laurance W. F. & Bierregaard Jr., R. O. editors. 1997. Tropical Forest Remnants:
Ecology, Management, and Conservation of Fragmented Communities. University
of Chicago Press, Chicago.
Laurance W.F., R.O. Bierregaard, C. Gascon, R.K. Didham, A.P. Smith, A.J. Lynam,
V.M. Viana, T.E. Lovejoy, K.E. Sieving, J.W. Sites, M. Andersen, M.D. Tocher,
E.A. Kramer, C. Restrepo, and C. Moritz. 1997. Tropical forest fragmentation:
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R.O. Bierregaard, eds. Tropical Forest Remnants: Ecology, Management, and
Conservation of Fragmented Communities. University of Chicago Press, Chicago.
Laurance W.F., S.G. Laurance, L.V. Ferreira, J.M. Rankin-de Merona, C. Gascon, and
T.E. Lovejoy. 1997. Biomass collapse in Amazonian forest fragments. Science
278:1117-1118.
Laurance W.F., K.R. McDonald, and R. Speare. 1996. Epidemic disease and the
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413.
Leakey M. 1988. Fossil evidence for the evolution of guenons. Pp. 54-78, in A. Gautier-
Hion, F. Bourliere, and J.P. Gautier, eds. A Primate Radiation: Evolutionary
Biology of the African Guenons. Cambridge University Press, Cambridge.
Lewis O.T. 2001. Effect of experimental selective logging on tropical butterflies.
Conservation Biology 15:389-400.


58
found only in undisturbed forest. The number of parasite species infecting individual red
colobus was greater in forest fragments compared to undisturbed forest (t = -5.785, P <
0.001, Figure 5-2).
For black-and-white colobus, the prevalence of infection with Trichuris sp., S.
fulleborni, Oespohagostomum sp., a dicrocoeliid liver fluke, E. coli, and E. histolytica did
not differ between animals in forest fragments and undisturbed forest (Table 5-2). Only
black-and-white colobus from forest fragments were infected with Ascaris sp. and
unknown strongyles (Table 5-2). There were no species of parasite found only in
undisturbed forest. The number of parasite species infecting individual black-and-white
colobus did not differ between forest fragments and undisturbed forest (t = -0.219, P =
0.827, Figure 5-2).
Infection Risk
Trichuris sp. eggs were more abundant in canopy plots (fragmented mean = 1.36
0.35 eggs/plot, undisturbed mean = 0.47 0.25 eggs/plot, t = -2.43, P = 0.022) and
ground vegetation plots (fragmented mean = 1.87 0.48 eggs/plot, undisturbed mean =
0.43 0.26 eggs/plot, t = -2.40, P = 0.026) from fragmented compared to undisturbed
forest. Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots
from fragmented compared to undisturbed forest (fragmented mean = 3.33 0.64
larvae/plot, undisturbed mean = 0.14 0.11 larvae/plot, t= -4.95, P < 0.001), but were not
found in canopy plots. No infective-stage primate parasites were identified from the soil
plots.
Colobus Population Dynamics
Ten of the 20 forest fragments censused contained red colobus and persisted for the
duration of the study (i.e., were not cleared). In these fragments, red colobus declined


Table 4-4. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Logged(n =125)
Undisturbed (n = 106)
Significance
Trichuris sp.
79
84
N.S.
Strongyloides fulleborni
4
3
N.S.
Oesophagostomum sp.
9
9
N.S.
Colobenterobius sp.
2
0
N.A.
Dicrocoeliid liver fluke
1
1
N.S.
Bertiella sp.
1
0
N.A.
Entamoeba coli
16
9
N.S
Entamoeba histolytica
16
9
N.S.
Overall
79
84
N.S.
N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence


59
from 163 individuals in 2000 to 131 individuals in 2003, a 20% reduction. Twelve of the
forest fragments censused contained black-and-white colobus and persisted for the
duration of the study. In these fragments, black-and-white colobus increased from 97
individuals in 2000 to 101 individuals in 2003, a 4% increase. Results of red colobus and
black-and-white colobus censuses over the past three decades in the K-30 compartment
of Kibale National Park demonstrate that densities of both colobus species are stable
(Chapman et al 2000).
Discussion
My results demonstrate that forest fragmentation has altered infection dynamics
resulting in higher densities of infective-stage parasites common to red colobus and
black-and-white colobus. Despite this higher infection risk for both species, only red
colobus manifested higher prevalence and richness of gastrointestinal parasite infections
and a higher number of parasite species infecting individuals in fragmented compared to
undisturbed forests. These results suggest that red colobus are more susceptible to
parasitic infection following forest fragmentation than black-and-white colobus.
Reduced food availability and diversity is likely the critical environmental stressor
responsible for this elevated susceptibility of red colobus to infection following forest
fragmentation. Compared to intact forest, fragments have been documented to have
higher rates of tree mortality (Mesquita et al. 1999), increased densities of trees with
wind- or water dispersed seeds, and reduced densities of trees with vertebrate-dispersed
seeds (Tabarelli et al. 1999), of which smaller fruited species predominate (Chapman and
Onderdonk 1998). These trends predict an overall reduction in food resources for
frugivorous and folivorous vertebrates in forest fragments. For species sensitive to
changes in food availability, resultant food stress may increase susceptibility to infection.


47
change is essential to promote land-use policy that is compatible with animal and human
health and biodiversity conservation.
Our understanding of how anthropogenic habitat change alters wildlife disease
dynamics is in its infancy. Our comprehension of this interplay will be greatly improved
by future research that investigate how selective logging and other forms of
anthropogenic habitat disturbance affect the rates and patterns of parasite and disease
transmission within and between species. In addition, studies are needed that explore how
nutritional state modulates the effects of parasites and the occurrence of disease in wild
populations. Identifying risk factors for disease transmission will improve the ability of
conservationists to make rational decisions about the risks and benefits of extraction and
management activities.


41
logged forest than undisturbed forest, their populations were in a state of recovery. In
contrast, the study found black-and-white colobus densities to be higher in logged forest
than in undisturbed forests.
The current study provides insights into the variable responses to logging observed
in these redtail guenon, red colobus, and black-and-white colobus populations. It is clear
that logging at Kibale has altered parasite dynamics resulting in higher densities of
infective-stage parasites common to both guenons and colobines. Despite this higher
infection risk for all three primate species, only redtail guenons manifest higher
prevalence and richness of gastrointestinal parasite infections and a higher mean number
of parasite species infecting individuals in logged compared to undisturbed forests.
These results suggest that guenons are more susceptible to parasitic infection following
selective logging than colobines.
The greater long-term impact of logging on guenon compared to colobine
populations may be a function of altered parasite dynamics in association with food
availability and animal nutrition and condition. Dietary stress may adversely affect
resistance to parasitic infection by reducing the effectiveness of the immune system
(Crompton 1991, Solomons and Scott 1994, Holmes, 1995, Milton 1996). As a result,
food shortages could result in higher parasite intensity, which in turn could increase
nutritional demands on the host and accentuate the effects of food shortages. Under such
conditions, nutritional status and parasitism could have synergistic effects on the host and
the individual effects of each factor would be amplified when co-occurring (Mihook et al.
1985, Keymer and Dobson 1987, Holmes 1995).


TABLE OF CONTENTS
Page
ACKNOWLEDGMENTS iii
LIST OF TABLES viii
LIST OF FIGURES x
ABSTRACT xi
CHAPTER
1 INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE
DYNAMICS 1
Overview 1
Human Disturbance and Primate Populations 2
Primate-Parasite Dynamics 5
Disturbance and Primate-Parasite Dynamics 6
Rationale 8
2 GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN
UGANDA 10
Introduction 10
Materials and Methods 11
Results 12
Nematoda 12
Cestoda 14
Trematoda 14
Protozoa 15
Effect of Season and Host Sex on Infection Prevalence 15
Variation in Prevalence among Sites throughout Africa 15
Discussion 16
3 GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF
UGANDA 21
Introduction 21
Materials and Methods 22
Results 23
v


98
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26
Bertiella sp. did not differ between colobus species (P > 0.1, Table 3-1). Since eggs of
this species are passed in proglottids, they are not mixed heterogeneously in feces.
Consequently, these prevalence values are likely an underestimation of prevalence.
Trematoda
A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,
operculated, golden-brown coloration). Eggs were found in feces of red colobus (46 X
24 pm) and eastern black-and-white colobus (43.8 1.1 X 23.6 1.4 pm). Prevalence of
Dicrocoelium sp. was higher for eastern black-and-white colobus than red colobus (X =
5.34, d.f. = 1, P< 0.025, Table 3-1).
Protozoa
Multinucleate cysts most closely resembling Entamoeba coli were found in the
feces of all colobus species and had a mean diameter of 18.1 1.0 pm for red colobus,
17.4 1.4 pm for eastern black-and-white colobus, and 17.6 1.3 pm for Angolan black-
and-white colobus. Prevalence of E. coli was higher for eastern black-and-white colobus
than red colobus (X2 = 4.28, d.f. = 1, P< 0.05, Table 3-1).
Cysts most closely resembling Entamoeba histolytica were found in the feces of all
colobine species and had a mean diameter of 13.2 1.1 pm for red colobus, 12.5 1.8
pm for eastern black-and-white colobus, and 12.7 1.6 pm for Angolan black-and-white
colobus. Prevalence of E. histolytica was higher for eastern black-and-white colobus
than red colobus (X2 = 14.68, d.f. = 1, P< 0.001, Table 3-1).
Ovoid cysts most closely resembling Giardia lamblia were only found in the feces
of red colobus and had a mean diameter of 11.9 1.8 pm (Table 3-1).


93
Mittermeier R.A. and D.L. Cheney. 1987. Conservation of primates and their habitats.
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forest. Journal of Applied Ecology 35:596-606.


81
strongyle) and two species infecting black-and-white colobus (Ascaris sp. and an
unidentified strongyle) are likely anthropozoonotic or epizootic in origin. These
parasites occur at high frequency in the human populations in the region, but are
absent from colobus within Kibale National Park, where the people and primates
interact at a reduced frequency.
5. This study demonstrated that an index of habitat degradation, stump density, best
explained the prevalence of strongyle and rhabditoid nematode infections in red
colobus in forest fragments in western Uganda. This coincided with a greater risk
of infection with Oesophagostomum sp.,a representative strongyle nematode, for
red colobus in the fragment with the highest stump density compared to the
fragment with the lowest stump density. Considering the potential role that these
nematode infections may play in red colobus declines in forest fragments, future
studies should investigate ways to mitigate alterations in infection dynamics in the
face of extraction.


61
Johnsen 1978). Even moderate intensities of Oesophogostomum sp. have proven
clinically important in stressed captive primates (Crestian and Crespeau 1975; Soulsby
1982). For example, nearly 30% of 70 guenons imported to Italy from Senegal died soon
after arrival from severe oesophogostomiasis (Roperto et al 1985). Secondary bacterial
infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent
complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of
parasites infecting red colobus in forest fragments may contribute to greater morbidity
and mortality in this colobus population compared to the population inhabiting
undisturbed forests.
The magnitude and prevalence of multiple-species infections in individuals can be
another useful indirect indicator that parasites may be impacting host populations.
Multiple-species infections are associated with a greater potential for morbidity and
mortality due to synergistic and competitive interactions occurring between parasite
species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sabelis 1995).
Consequently, the elevated frequency and number of multiple-species infections observed
in red colobus in forest fragments may contribute to greater morbidity and mortality in
this colobus population compared to the population inhabiting undisturbed forests.
My results demonstrate that humans, and potentially livestock, are exposing
colobus in forest fragments to novel pathogens. Four species infecting red colobus
(Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified strongyle)
and two species infecting black-and-white colobus (Ascaris sp. and an unidentified
strongyle) are likely anthropozoonotic or epizootic in origin. These parasites occur at
high frequency in the human populations in the region (NEMA 1997), but are absent


14
skin or by necropsy (Ashford et al. 2000). Consequently, these prevalence values may be
underestimations of actual prevalence.
Spiruroidea: Eggs that most closely resemble Streptopharagus sp. (symmetrical,
larvated, thick-shelled) were found in feces of all guenon species, except lhoesti
monkeys, and measured 38.5 2.1 X 24.3 1.1 pm for redtail guenons, 40.1 1.9 X
25.0 1.3 pm for blue monkeys, and 41.7 1.8 X 25.6 1.5 pm for vervets. Prevalence
of Streptopharagus sp. did not differ (P > 0.05) between redtail guenons (18%) and blue
monkeys (14%) (P > 0.05, Table 2-1).
Cestoda
Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed
oncosphere) were found in feces of only 1 redtail guenon, and measured 40-43 X 48-51
pm (n = 4); and no proglottids were detected through macroscopic inspection of feces
(Table 2-1). Since eggs of this species are passed in proglottids, they are not mixed
heterogeneously in feces. Consequently, these prevalence values may be gross
underestimations of actual prevalence.
Trematoda
A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,
operculated, golden-brown coloration). Eggs were found in feces of all guenon species
except lhoesti monkeys, and measured 45.8 1.1 X 24.2 1.0 pm for redtail guenons,
44 X 24 pm for blue monkeys, and 46 X 24 pm for vervets. Prevalence of this trematode
did not differ (P > 0.05) between redtail guenons (2%) and blue monkeys (3%) (Table 2-
1)-


86
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Michigan, Ann Arbor, MI.
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Bioscience 45:456-464.
Ganzhom J.U. 1995. Low-level forest disturbance effects on primary production, leaf
chemistry, and lemur populations. Ecology 76:2048-2096.


5
en
>
O
en
O
C-
O
es
4
3
2
*
i
o
HMHH
(n = 561)
(n = 388)
Red Colobus
Undisturbed
Fragmented
T
(n = 100)
Black-and-White Colobus
as
as
Figure 5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus tephrosceles), and black-and-white colobus
{Colobus guereza) in undisturbed and fragmented forest Western Uganda.


71
Florida where they were examined for nematode eggs and larvae using concentration by
sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Nematodes were
counted and identified on the basis of egg color, shape, contents, and size. Measurements
were made to the nearest 0.1 micron SD using an ocular micrometer fitted to a
compound microscope. Coprocultures and necropsies (MAFF 1979) were used to match
nematode eggs to larvae and adult worms for positive identification.
Infection Risk Assessment
To obtain an index of infection risk, I determined infective-stage parasite densities
for canopy vegetation, ground vegetation, and soil plots from fragments with high stump
density (Kiko 3) and low stump density (Nkuruba). From January to August 2002,1
collected thirty 1 m3 vegetation plots at a height of 12 m from canopy trees used within
the previous two hours by red colobus; 15 from each fragment. Canopy access for plot
collection was facilitated by single rope climbing technique (Mitchell, 1982; Laman,
1995, Houle et al. 2004). Thirty 1 m3 ground vegetation plots were collected below all
trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches) were collected
within randomly selected ground vegetation plots, 10 from forest fragments and 10 from
undisturbed forest. I used a modified sedimentation technique to recover infective-stage
parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using a
modified Baermann method (Sloss et al. 1994). Samples were examined by dissecting
and compound scope, and infective-stage individuals of the most prevalent strongyle
nematode, Oespohagostomum sp. (L3 larvae) were counted.
Fragment Characteristics
Forest fragment attributes quantified included fragment size, fragment type,
distance to Kibale, distance to the nearest fragment, trees/ha, tree species/ha, tree


62
from colobus within Kibale National Park, where the people and primates interact at a
reduced frequency. In addition, the majority of colobine parasites appear to be
generalists and occur in the local human population (NEMA 1997). These are the
pathogens of greatest concern for rare species, such as the red colobus (Lafferty and
Gerber 2002). Humans and livestock may act as reservoirs, maintaining a high infection
risk for parasites that are detrimental to red colobus, even as red colobus densities decline
toward extinction (McCallum and Dobson 2002). Likewise, considering the extensive
overlap in parasite communities between the colobine species, black-and-white colobus
may also be acting as reservoirs for most red colobus parasites. Consequently, it will be
important to recognize the importance of generalist parasites within a community context
to preserve sensitive species, such as the endangered red colobus.
Our understanding of how anthropogenic habitat change alters wildlife disease
dynamics is in its infancy. Our comprehension of this interplay will be greatly improved
by future research that investigates how forest fragmentation and other forms of
anthropogenic habitat disturbance affect the rates and patterns of parasite transmission
within and among species. In addition, studies are needed that explore if and how
nutritional state modulates the effects of parasites and the occurrence of disease in wild
populations. Identifying risk factors for disease transmission will improve the ability of
conservationists to make rational decisions about the risks and benefits of extraction and
management activities.


33
but increased following similar intensity logging at another site in Uganda (Plumptre and
Reynolds 1994; Chapman et al. 2000).
Ninety percent of primate species are restricted to the tropics, and the majority are
forest dependent (Chapman and Peres 2001). Consequently, with 5 to 6 million ha of
tropical forest selectively logged each year (FAO 1990; FAO 1999), it is not surprising
that primates have been the focus of much research concerning the impact of logging on
biodiversity (Johns and Skorupa 1987; Johns 1997; Struhsaker 1997; Chapman et al.
2000). Although logging is known to negatively impact the abundance of some primate
species, the proximate mechanism for these declines remains unknown. Implied
mechanisms include altered ranging patterns (Johns 1997) and reduced food-tree density
(Skorupa 1988; Struhsaker 1997; Chapman et al. 2000). However, contrasting sites to
arrive at generalities is often difficult, as some areas experience increased hunting
pressure after logging, while others areas do not (Mittermeier 1987; Peres 1990; Oates
1994; Robinson and Bennett 2000). Support for the operation of particular mechanisms
for primate declines following logging is largely indirect and it is unlikely that a single
correlate will explain the complex relationship between primate declines and logging-
induced ecological change. The potential role of parasites and infectious disease in such
primate population declines remains largely unexplored.
Helminthic and protozoal parasites can impact host survival and reproduction
directly through pathological effects and indirectly by reducing host condition (Chandra
and Newbeme 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop
and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous
abortion, congenital malformations, and death (Chandra and Newbeme 1977;


83
Bierreggard R.O., T.E. Lovejoy, V. Kapos, A. Santos, and R.W. Hutchings. 1992. The
biological dynamics of tropical rainforest fragments. Bioscience 42:859-866.
Boyce M.S. 1990. The red queen visits sage grouse leks. American Zoologist 30:263-
270.
Brack M. 1987. Agents Transmissible from Simians to Man. Springer-Verlag, Berlin.
Brieger W.R. 1996. Health education to promote community involvement in the control
of tropical diseases. Biotropica 61:93-106.
Brown H.W. and F.A. Neva. 1983. Basic Clinical Parasitology. Fifth edition. Appleton-
Century-Crofts, Norwalk, CT.
Brugiere D. 1998. Population size of the black colobus monkey (Colobus satanas) and
the impact of logging in the Lope Reserve, Central Gabon. Biological Conservation
86:15-20.
Bundy D.A.P. and M.H.N. Golden. 1987. The impact of host nutrition on gastrointestinal
helminth populations. Parasitology 95:623-635.
Butynski T.M. 2002. Conservation of the guenons: an overview of status, threats, and
recommendations. Pp. 411-424, in M.E. Glenn and M. Cords, eds. The Guenons:
Diversity and Adaptation in African Monkeys. Kluwer Academic/Plenum
Publishers, New York.
Camaniti B. 1984. Parasites of the Digestive System of Nonhuman Primates: A
Supplemental Bibliography, 1970-1984. Regional Primate Research Center,
Seattle, WA.
Camaniti B. 1987. Parasites of the Digestive System of Nonhuman Primates: A
Supplemental Bibliography, 1982-1987. Primate Information Center, Regional
Primate Research Center, Seattle, WA.
Chandra R. 1983. Nutrition, immunity, and infection: present knowledge and future
directions. The Lancet 1:688-691.
Chandra R.K. and P.M. Newbeme. 1977. Nutrition, Immunity, and Infection. Plenum
Press, New York.
Chapman C.A., S.R. Balcomb, T.R. Gillespie, J.P. Skorupa, and T.T. Struhsaker. 2000.
Long-term effects of logging on primates in Kibale National Park, Uganda: A 28-
year comparison. Conservation Biology 14:207-217.
Chapman C.A. and L.J. Chapman. 1997. Forest regeneration in logged and unlogged
forests of Kibale National Park, Uganda. Biotropica 29:396-412.


27
Effect of Season and Host Sex on Infection Prevalence
While prevalence did not correlate significantly with monthly rainfall for any
parasite species infecting red colobus (P > 0.077) or eastern black-and-white colobus (P
> 0.081), variation over the year was evident (Figure 3-1).
Prevalence of S. fulleborni was higher in adult male red colobus compared to adult
females (X2 = 6.19, d.f. = 2, P < 0 .05). However, prevalence did not differ for any other
shared parasite species between age and sex classes (P > 0.05).
Discussion
To my knowledge, this is the first report of gastrointestinal parasites from wild
populations of colobus monkeys. The similarities in gastrointestinal parasite faunas
among the colobus of Uganda demonstrate that generalist parasites predominate. This
supports the suggestion that in communities comprised of closely related species, cross
species interaction may be an important source of infection risk (Ezenwa 2003). This
may be one reason that colobines associate with unrelated guenons far more than with
other colobus species (Chapman and Chapman 2000). It is also important to note that
many of the species infecting colobines in Uganda occur at high frequency in the human
populations in the region (NEMA 1997). Consequently, zoonotic and/or
anthropozoonotic transmission may occur and may be promoted by various forms of
anthropogenic disturbance.
Despite the great correspondence in parasite faunas among colobines, prevalence
varied greatly with red colobus having the lowest prevalence and Angolan black-and-
white colobus having the highest prevalence. Prevalence is likely affected by complex
interactions among environmental, demographic, genetic, and behavioral factors, making
it difficult to explain this variation in prevalence. However, one relationship is


88
Hamer K.C., J.K. Hill, S. Benedick, N. Mustaffa, T.N.Sherratt, M. Maryati, and V.K.
Chey. 2003. Ecology of butterflies in natural and selectively logged forests of
northern Borneo: the importance of habitat heterogeneity. Journal of Applied
Ecology 40:150-162.
Hastings B.E., D. Kenny, L.J. Lowenstine, and J.W. Foster. 1991. Mountain gorillas and
measles: ontogeny of a wildlife vaccination program. Proceedings AAZA Annual
Meeting. Pp 198-205.
Hausfater G. and B.J. Meade. 1982. Alteration of sleeping groves by yellow baboons
(Papio cynocephalus) as a strategy for parasite avoidance. Primates 23:287-297.
Hausfater G.and D.F. Watson 1976. Social and reproductive correlates of parasite
emissions by baboons. Nature 262:688-689.
Heydon M.J. and P. Bulloh. 1997. Mousedeer densities in a tropical rainforest: the impact
of selective logging. Journal of Applied Ecology 34:484-496.
Hochachka V.W. and A. A. Dhondt. 2000. Density-dependent decline of host abundance
resulting from a new infectious disease. Proceedings of the National Academy of
Science 97:5303-5306.
Holmes D.D., S.D. Kosanke S.D., G.L. White, and W.B. Lemmon. 1980. Fatal
enterobiasis in a chimpanzee. Journal of the American Veterinary Medicine
Association 177:911-913.
Holmes J.C. 1995. Population regulation: a dynamic complex of interactions. Wildlife
Research 22:11-20.
Holmes J.C. 1996. Parasites as threats to biodiversity in shrinking ecosystems.
Biodiversity Conservation 5:975-983.
Horii Y. and M. Usui. 1985. Experimental transmission of Trichuris ova from monkey to
man. Transactions of the Royal Society of Tropical Medicine and Hygiene 79:423.
Houle A., C.A. Chapman, and W. Vickery. 2004. Tree climbing strategies for primate
ecological studies. International Journal of Primatology 25:237-260.
Hudson P.J. 1986. The effect of a parasitic nematode on the breeding production of red
grouse. Journal of Animal Ecology 55:85-92.
Hudson P.J., A.P. Dobson, and D. Newborn. 1992. Do parasites make prey vulnerable to
predation: red grouse and parasites. Journal of Animal Ecology 61: 681-692.
Huffman M.A., S. Gotoh, L.A. Turner, M. Hamai, and K. Yoshida. 1997. Seasonal trends
in intestinal nematode infection and medicinal plant use among chimpanzees in the
Mahale Mountains, Tanzania. Primates 38:111-125.


29
eastern black-and-white colobus (n = 7). This differs from my results, which demonstrate
that colobines are susceptible to protozoan infection. However, my results reveal that
protozoan prevalence for colobines is low compared to other primate species examined
by Freeland (1977) (e.g., chimpanzees, baboons). Accordingly, it is likely that greater
sampling effort during this earlier study would have yielded findings similar to my own.
This study contributes baseline data on the patterns of parasitic infection in wild
colobus monkeys, providing a first step toward an index of population health and disease
risk assessment for conservation and management plans of threatened and endangered
colobus populations. I documented that the vast majority of gastrointestinal parasites of
wild colobus may be zoonotic or anthropozoonotic. Accordingly, future studies are
needed to determine risks of cross-transmission. Mechanisms to reduce such risks may
promote human health, livestock production, and local support for conservation.
Gastrointestinal parasite classification by fecal analyses is weak by its very nature.
However it is the only responsible method to approach threatened species. Future studies
employing molecular analyses and opportunistic necropsies are needed to improve our
classification of the gastrointestinal parasites of guenons, as well as to improve our
understanding of the risks of epizootic and zoonotic transmission.


40
with Colobenterobius sp. (Table 4-3). The mean number of parasite species infecting
individual red colobus did not differ between logged and undisturbed forest (t = 1.32, P =
0.186, Figure 4-1).
The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum
sp., the dicrocoeliid liver fluke, E. coli, and E. histolytica did not differ between black-
and-white colobus from logged and undisturbed forest (Table 4-4). Only black-and-white
colobus from logged forest were infected with Colobenterobius sp. and Bertiella sp.
(Table 4-4). The mean number of parasite species infecting individual black-and-white
colobus did not differ between logged and undisturbed forest (t = 0.64, P = 0.524, Figure
4-1).
Infection Risk
Trichuris sp. eggs were more abundant in canopy plots (Disturbed Mean = 1.43
0.20, Undisturbed Mean = 0.47 0.25, t = -2.66, P = 0.013) and ground vegetation plots
(Disturbed Mean = 4.21 0.13, Undisturbed Mean = 0.43 0.96 t = -3.56, P = 0.003)
from logged compared to undisturbed forest. Oesophagostomum sp. L3 larvae were more
abundant in ground vegetation plots from logged compared to undisturbed forest
(Disturbed mean = 3.93 1.23, Undisturbed mean = 0.14 0.11, t= -3.14, P = 0.008), but
were not found in canopy plots. No infective-stage primate parasites were identified
from the soil plots.
Discussion
A recent study demonstrated that group densities for redtail and blue guenons at
Kibale were lower in logged forest than undisturbed forest and that their populations
declined between censuses conducted 12 and 28 years after logging (Chapman et al.
2000). Although Chapman et al. (2000) found red colobus densities to be lower in


39
by dissecting and compound scope. Infective-stage primate parasites were identified and
counted.
Statistical Analyses
I employed chi-square tests of independence to compare the prevalence of infection
between the logged and undisturbed forests for overall and specific infections for each of
the three primate species. Independent sample t-tests were performed to compare the
mean number of parasite species infecting individual primates and the density of
infective-form parasites in vegetative plots between the logged and undisturbed forests
(SPSS, version 10, 1999).
Results
Infection Prevalence and Richness
Descriptions of taxa, mode of infection, and associated pathology for each parasite
species recovered can be found in Table 4-1. The prevalence of infection with Trichuris
sp., Streptopharagus sp., Strongyloid.es fulleborni, Oespohagostomum sp., Entamoeba
coli, E. histolytica, and Iodameoba buetschlii was higher for redtail guenons from logged
forest compared to guenons from undisturbed forest (Table 4-2). Only redtail guenons
from logged forest were infected with Enterobius sp., a dicrocoeliid liver fluke, Bertiella
sp., Giardia lamblia, and Chilomastix mesnili (Table 4-2). There were no species of
parasite found only in undisturbed forest. The mean number of parasite species infecting
individual redtail guenons was greater in logged compared to undisturbed forest (t = 5.74,
P< 0.001, Figure 4-1).
The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum
sp., E. coli, and E. histolytica did not differ between red colobus from logged and
undisturbed forest (Table 4-3). Only red colobus from undisturbed forest were infected


LIST OF FIGURES
Figure page
2-1 Inter-monthly variation in parasite infection prevalence of redtail guenons and
rainfall at Kibale National Park, Uganda 20
3-1 Inter-monthly variation in parasite infection prevalence of colobus monkeys and
rainfall at Kibale National Park, Uganda 31
4-1 Mean number of parasite species infecting individual redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-and-
white colobus (Colobus guereza) in undisturbed and logged forest at Kibale
National Park, Uganda 52
5-1 Conceptual model of proposed mechanism for population declines in forest 65
5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus
tephrosceles), and black-and-white colobus (Colobus guereza) in undisturbed and
fragmented forest Western Uganda 66
x


Table 6-3.Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus monkeys (Piliocolobus tephrosceles) and
attributes of the forest fragments they inhabit near Kibale National Park, Uganda
Oesophagostomum sp. Unidentified Strongyle Strongyloides fullebomi Strongyloides stercoralis Collective
Fragment Size
-0.581 (p = 0.101)
-0.730 (p = 0.025) *
-0.777 (p = 0.014)**
-0.835 (p = 0.005) **
-0.811 (p = 0.008)
Fragment Type
-0.220 (p = 0.570)
-0.409 (p = 0.274)
0.049 (p = 0.901)
-0.014 (p = 0.971)
-0.185 (p = 0.634)
Distance to Kibale
-0.336 (p = 0.377)
-0.393 (p = 0.296)
-0.328 (p = 0.389)
-0.401 (p = 0.285)
-0.417 (p = 0.264)
Nearest Fragment
-0.204 (p = 0.598)
0.285 (p = 0.458)
-0.121 (p = 0.757)
-0.291 (p = 0.448)
-0.019 (p = 0.962)
Trees / ha
0.201 (p = 0.605)
0.109 (p = 0.780)
0.142 (p = 0.715)
0.422 (p = 0.258)
0.199 (p = 0.608)
Tree sp. / ha
-0.128 (p = 0.744)
-0.199 (p = 0.607)
-0.226 (p = 0.560)
0.012 (p = 0.976)
-0.184 (p = 0.635)
Red Colobus / ha
0.239 (p = 0.536)
0.010 (p = 0.980)
0.442 (p = 0.234)
0.672 (p = 0.047) *
0.437 (p = 0.240)
Colobines / ha
0.459 (p = 0.214)
0.267 (p = 0.487)
0.367 (p = 0.331)
0.691 (p = 0.039) *
0.511 (p = 0.160)
Stumps / ha
0.811 (p = 0.008) **
0.766 (p = 0.016)**
0.869 (p = 0.002) **
0.954 (p< 0.001)**
0.920 (p< 0.001)
(n 9 for all comparisons, Pearson Correlation and corresponding P-value provided)


300
250
200
150
100
50
0
Month
Figure 2-1. Inter-monthly variation in parasite infection prevalence of redtail guenons and rainfall at Kibale National Park, Uganda
Rainfall (mm)


EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS
By
THOMAS R. GILLESPIE
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF
DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
2004

Copyright 2004
by
Thomas R. Gillespie

ACKNOWLEDGMENTS
I thank my advisor, Colin Chapman, whose support and assistance were invaluable
during this work. His expertise and enthusiasm provided a solid foundation for this study.
I owe much to my committee members (Drs. Sue Boinski, Lauren Chapman, Ellis
Greiner, and Michael Huffman) for their advice and support throughout this venture.
Drs. Andy Dobson, Donald Forrester, Robert Holt, William Karesh, Joanna Lambert,
Arthur Mugisha, Thomas Struhsaker, and the honorable Betty Udongo shared insights
that improved this work.
I am grateful to Dennis Sebugwawo and all employees of the Kibale Fish and
Monkey Project for their hard work and dedication. I am grateful to Stacey Bonovitch,
Lauren Castleberry, Brian Davidson, John Davis, Jennifer Davis-Summer, Erin Ehmke,
Kristen Guttmann, Sarah Hawkins, Joe Mahoney, Anjan Patel, Michelle Roman, May
Stewart, Gregory Zhelesnik, and Jennifer Zipser for their assistance in the laboratory. I
thank my many colleagues at Kibale National Park, Uganda, and the University of
Florida who have shared insight, advice, friendship, and humor. Especially Evelina
Jagminaite who saw me through much of this work.
I am ever grateful to my parents, Robert and Margaret Gillespie, who have been a
constant source of encouragement and support throughout my life.
This research has been supported by grants from the National Center for
Environmental Research of the United States Environmental Protection Agency (STAR
Fellowship), the National Science Foundation (grant number SBR-990899), the Wildlife
iii

Conservation Society, and the Ford Foundation. Permission to conduct this research was
provided by the Uganda National Research Council, Office of the President, the Uganda
Wildlife Authority, and Makerere University.
This dissertation is dedicated to Brian Riewald, whose spirit and character will
always be with me.
IV

TABLE OF CONTENTS
Page
ACKNOWLEDGMENTS iii
LIST OF TABLES viii
LIST OF FIGURES x
ABSTRACT xi
CHAPTER
1 INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE
DYNAMICS 1
Overview 1
Human Disturbance and Primate Populations 2
Primate-Parasite Dynamics 5
Disturbance and Primate-Parasite Dynamics 6
Rationale 8
2 GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN
UGANDA 10
Introduction 10
Materials and Methods 11
Results 12
Nematoda 12
Cestoda 14
Trematoda 14
Protozoa 15
Effect of Season and Host Sex on Infection Prevalence 15
Variation in Prevalence among Sites throughout Africa 15
Discussion 16
3 GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF
UGANDA 21
Introduction 21
Materials and Methods 22
Results 23
v

Nematoda 23
Cestoda 25
Trematoda 26
Protozoa 26
Effect of Season and Host Sex on Infection Prevalence 27
Discussion 27
4LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN
AFRICAN PRIMATE POPULATIONS 32
Introduction 32
Materials and Methods 35
Study Site 35
Fecal Sampling and Analysis 37
Infection Risk Assessment 38
Statistical Analyses 39
Results 39
Infection Prevalence and Richness 39
Infection Risk 40
Discussion 40
5ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES
IN FOREST FRAGMENTS 53
Introduction 53
Materials and Methods 55
Study Site 55
Fecal Sampling and Analysis 55
Infection Risk Assessment 56
Colobus Surveys 57
Statistical Analyses 57
Results 57
Infection Prevalence and Richness 57
Infection Risk 58
Colobus Population Dynamics 58
Discussion 59
6VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST
FRAGMENT ATTRIBUTES 67
Introduction 67
Materials and Methods 70
Study Site 70
Fecal Sampling and Analysis 70
Infection Risk Assessment 71
Fragment Characteristics 71
vi

Results 73
Discussion 75
7 SUMMARY AND CONCLUSIONS 80
LIST OF REFERENCES 82
BIOGRAPHICAL SKETCH 99
vii

LIST OF TABLES
Table
page
2-1 Prevalence (%) of gastrointestinal helminth parasite infections in guenons of
western Uganda 19
3-1 Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys
of Uganda 30
4-1 Mode of infection, morbidity, and mortality associated with gastrointestinal
parasites infecting redtail guenon (Cercopithecus ascanius), red colobus
(Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda 48
4-2 Prevalence (%) of gastrointestinal parasite infections in redtail guenons
(Cercopithecus ascanius) from logged and undisturbed forests in Kibale National
Park, Uganda 49
4-3 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from logged and undisturbed forests in Kibale National Park, Uganda50
4-4 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from logged and undisturbed forests in Kibale National Park,
Uganda 51
5-1 Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus
tephroceles) from forest fragments and undisturbed forests in Kibale National Park,
Uganda 63
5-2 Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus
(Colobus guereza) from forest fragments and undisturbed forests in Kibale
National Park, Uganda 64
6-1 Physical and biological attributes of forest fragments with red colobus
(Piliocolobus tephroceles) populations near Kibale National Park, Uganda 77
6-2 Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus
monkeys (Piliocolobus tephroceles) in forest fragments near Kibale National Park,
Uganda 78
viii

6-3 Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus
monkeys (Piliocolobus tephrosceles) and attributes of the forest fragments they
inhabit near Kibale National Park, Uganda
79

LIST OF FIGURES
Figure page
2-1 Inter-monthly variation in parasite infection prevalence of redtail guenons and
rainfall at Kibale National Park, Uganda 20
3-1 Inter-monthly variation in parasite infection prevalence of colobus monkeys and
rainfall at Kibale National Park, Uganda 31
4-1 Mean number of parasite species infecting individual redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-and-
white colobus (Colobus guereza) in undisturbed and logged forest at Kibale
National Park, Uganda 52
5-1 Conceptual model of proposed mechanism for population declines in forest 65
5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus
tephrosceles), and black-and-white colobus (Colobus guereza) in undisturbed and
fragmented forest Western Uganda 66
x

Abstract of Dissertation Presented to the Graduate School
of the University of Florida in Partial Fulfillment of the
Requirements for the Degree of Doctor of Philosophy
EFFECTS OF HUMAN DISTURBANCE ON PRIMATE PARASITE DYNAMICS
By
Thomas R. Gillespie
August 2004
Chair: Colin A. Chapman
Major Department: Zoology
Emerging infectious diseases have raised global awareness of the impact ecological
change can have on biodiversity conservation and wildlife and human health. This study
improves our understanding of this interplay by examining effects of logging and forest
fragmentation on parasite dynamics in an African primate community. From August
1997 to July 2003, 2,017 fecal samples were collected to compare gastrointestinal
parasite infections of red colobus (Piliocolobus tephroceles), black-and-white colobus
(Colobus guereza), and redtail guenon (Cercopithecus ascanius) populations from logged
(all), fragmented (only colobines), and undisturbed forests (all) at Kibale National Park,
Uganda. Dynamics of red colobus infection with strongyle and rhabditoid nematodes
were examined in relation to forest fragment attributes. Helminth eggs, larvae, and
protozoan cysts were identified using sodium-nitrate flotation and fecal sedimentation.
Coprocultures and necropsies facilitated identification. Infection-risk was quantified by
modified sedimentation technique, comparing densities of infective-stage parasites from
canopy and ground vegetation plots in logged, fragmented, and undisturbed forest.
xi

Prevalence and richness of gastrointestinal parasite infections and magnitude of
multiple infections were greater for guenons in logged than in undisturbed forest, but
these parameters did not differ between forest types for either colobine. Infection-risk
was greater for primates in logged compared to undisturbed forest. Prevalence and
richness of gastrointestinal helminth and protozoan parasite infections and frequency of
multiple infections were greater for red colobus in fragmented than in undisturbed forest,
but these parameters did not differ between these areas for black-and-white colobus.
Infection-risk was greater for colobines in fragmented compared to undisturbed forest.
Inter-fragment comparisons examining 10 potential factors demonstrated that an index of
degradation, tree-stump-density, strongly influenced prevalence of strongyle and
rhabditoid nematodes. Infection risk was also higher in the fragment with highest stump-
density compared to the fragment with lowest stump-density. Fragment size and
colobine density were correlated to prevalence for some nematodes, but in multiple
regression analyses with stump-density, these variable did not explain a significant
amount of variance.
These results demonstrate that selective logging and forest fragmentation have the
capacity to affect parasite infection dynamics in some African primate species. These
changes in infection dynamics may play a role in observed primate declines.
xii

CHAPTER 1
INTRODUCTION: HUMAN DISTURBANCE AND PRIMATE-PARASITE
DYNAMICS
Overview
Tropical forests, although covering only 6% of Earth's arable surface, account for
nearly 50% of all known species (National Research Council 1992). Less than 5% of
tropical forests are legally protected (Redford 1992; Oates 1996; Chapman et al. 2000)
and unprotected forests are being degraded at staggering rates (FAO 1999; Chapman and
Peres 2001). Consequently, conservation of many tropical forest species (such as
primates) will depend, at least in part, on the capacity of disturbed areas outside of
reserves to support their populations.
Ninety percent of primate species are restricted to the tropics (Mittermeier and
Cheney 1987), and more than half of primate species are threatened by extinction
(Chapman and Peres 2001). Thus, primates represent an ideal taxa for studying the
effects of human disturbance in tropical forests. Although human disturbance is known
to negatively impact primate populations, little is known about the mechanisms
responsible for such effects. One such mechanism may be infection dynamics.
Emerging tropical diseases (such as AIDS and Ebola) have raised global awareness
of the strong linkage between biodiversity conservation and the health of animal and
human populations (Meffe 1999; Daszak et al. 2000, 2001). To effectively understand
the dynamics of emerging diseases, we must evaluate the interplay among alteration and
fragmentation of tropical forests, wildlife-human disease linkages, and the ecology of
1

2
novel diseases. My study addresses an important aspect of these questions by examining
the effects of selective logging and forest fragmentation on primate-parasite dynamics in
an African tropical forest.
To provide background information on the framework of the research, this
introduction reviews the patterns of human disturbance and their impacts on primate
populations. Little is known about the mechanisms by which human disturbance impacts
primate populations and ecosystem processes. My study examines one potential
mechanism, primate-parasite dynamics. Since it is likely that pathogens and other factors
interact to produce an effect on primate populations, I provide background on human
disturbance and primate populations, and discuss how this may relate to primate-parasite
dynamics. This is followed by the objectives, rationale, methodology, and research
implications of my work.
Human Disturbance and Primate Populations
Forest fragmentation and selective logging dominate habitat-modification patterns
throughout the tropics (Chapman et al. 2000; Chapman and Peres 2001) and have
detrimental effects on most primate populations (Skorupa 1988; Bierregaard et al. 1992;
Bennett and Dahaban 1995; Chapman et al. 2000; Onderdonk and Chapman 2000). With
respect to forest fragmentation, primate species richness is lower in forest fragments
compared to equivalent areas of continuous forest (Bierregaard et al. 1992; Onderdonk
and Chapman 2000); primate species richness is typically higher in large compared to
small fragments (Bierregaard et al. 1992; Estrada et al. 1994; but see Onderdonk and
Chapman 2000); and primate densities typically are higher in large compared to small
fragments (Estrada and Coates-Estrada 1996; Chiarello 2000; but see Onderdonk and

3
Chapman 2000). Thus, forest fragmentation appears to negatively impact most primate
communities and species.
The impact of selective logging on primate populations depends greatly on the
intensity of the logging and the species in question. Low-intensity logging (5-20% of
trees destroyed) appears to be compatible with primate conservation (Johns and Skorupa
1987; Ganzhom 1995; Oates 1996; Brugiere 1998; Chapman et al. 2000). For example,
Ganzhom (1995) determined that low-intensity logging of forests in Madagascar
(affecting less than 10% of forest area) corresponds with an increase in abundance of all
lemur species (significantly so for three of seven species). Moreover, studies from
Kibale National Park in Uganda demonstrate that primate densities in low-intensity
logged forest are no different from primate densities in unlogged forest (Skorupa 1988;
Chapman et al. 2000). Consequently, low-intensity, selective logging potentially offers a
land-use option compatible with primate conservation.
In contrast, high-intensity logging (>50% of trees destroyed), the most common
form of logging in the tropics, appears to be detrimental to most primate populations
(Skorupa 1988; Bennett and Dahaban 1995; Chapman et al. 2000). For example, Bennett
and Dahaban (1995) found that high-intensity logging resulted in a 35-70% decline in
gibbon (Hylobates muelleri) and langur (Presbytis sp.) populations in Sarawak. Skorupa
(1988) demonstrated that 12 years after high-intensity logging, group densities of red
colobus (Piliocolobus tephrosceles) and red-tail guenons (Cercopithecus ascanius) were
lower compared to those in unlogged forest at Kibale National Park, Uganda. Chapman
et al. (2000) reveals that even 28 years after logging in the system examined by Skorupa
(1988), red-tail group densities were still lower in high-intensity logged forest compared

4
to unlogged forest. Moreover, group densities of Cercopithecus ascanius and C. mitis in
high-intensity logged forest continued to decline even 28 years after logging (Chapman et
al. 2000). In contrast, the density of eastern black-and-white colobus (Colobus guereza)
was not lower in logged compared to undisturbed forest at both 12 and 28 years after
logging (Skorupa 1988, Chapman et al. 2000). Thus, although some primate species may
cope well with high-intensity selective logging, the majority of primates fair poorly.
Although forest fragmentation and high-intensity, selective logging are known to
negatively impact primate abundance and species richness, little is known about the
proximate mechanisms responsible for such effects. To successfully combat species loss
in such systems, we must understand the underlying mechanisms of species loss. Parasite
dynamics may be one such mechanism.
Animal populations are largely regulated by three factors: availability of quality
food, predation, and infectious disease (Lack 1954; Minchella and Scott 1991; Dobson
1995). While a great deal of research has focused on the effects of food availability and
predation on primate abundance (Struhsaker 1976; Milton 1982; Isbell 1990; Struhsaker
and Leaky 1990; Chapman and Chapman 1999), the role of infectious disease has
remained largely unexplored (Stuart and Strier 1995). Forest fragmentation and high-
intensity, selective logging may alter primate-parasite dynamics (resulting in higher rates
of primate mortality, lower reproductive rates, and debilitation). Consequently, an
understanding of how these manifestations of human disturbance affect primate-parasite
dynamics could be of central importance in designing effective conservation and
management plans.

5
Primate-Parasite Dynamics
Gastrointestinal parasites infecting mammals are commonly transmitted through
contact with the free-living stages, ova, or larvae. This may involve contact with
contaminated food, water, fecal material, or soil (with vertebrate or invertebrate vectors),
or may involve direct contact with infected individuals (Brown and Neva 1983).
Parasites impact host survival and reproduction directly through pathological effects, and
indirectly by reducing host condition (Chandra and Newbeme 1977; Hart 1988, 1990,
1992; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Despommier et al.
1995; Coop and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage,
spontaneous abortion, congenital malformations, and death (Chandra and Newbeme
1977; Despommier et al. 1995). Less severe infections may impair nutrition; may
increase energy expenditure; or may impair travel, feeding, escape from predators, and
competition for resources or mates (resulting in mortality or lower fitness) (Boyce 1990;
Dobson and Hudson 1992; Hudson et al. 1992; Coop and Holmes 1996; Hart 1988, 1990,
1992). Through these proximate mechanisms, parasites can ultimately regulate host
populations (Gregory and Hudson 2000; Hochachka and Dhondt 2000) or cause short
term reductions in population size (Collias and Southwick 1952; Work et al. 1957).
Few studies have investigated the effects of parasite infections on wild primate
populations. However, evidence suggests that parasite infections can lead to primate
mortality. For example, Ohsawa (1979) and Dunbar (1980) demonstrated that larval
cestode infections contributed to high mortality rates for immature and older gelada
baboons (Theropithecus gelada). Several studies have demonstrated endoparasitic,
ectoparasitic, and viral epidemics in great ape populations in areas near human settlement
(Ashford et al. 1990; Hastings et al 1991; Kortlandt 1996; Meader et al. 1997; Pussey

6
1998). Each of these epidemics was potentially anthropozoonotic, meaning that the apes
were potentially infected by contact with humans. Yellow fever was implicated as the
cause of a 50% decline in the howling monkey (Alouatta palliata) population on Barro
Colorado Island, Panama, between 1933 and 1951 (Collias and Southwick 1952). Later
studies of this same howling monkey population suggested that heavy botfly infestations
(Alouattamyia baeri), in conjunction with food limitation, were limiting monkey densities
(Smith 1977; Milton 1996). Interestingly, Barro Colorado Island was isolated from a
much larger area of continuous disturbed forest after the damming of Lake Gatun during
the formation of the Panama Canal, and is hence the result of large-scale human
disturbance. The predominance of cases of population-level effects of parasites on
primates from human-disturbed systems suggests that populations in disturbed habitats
may be more vulnerable to parasites. However, more studies will be needed to confirm
this, since few studies have expressly looked at such issues in undisturbed systems.
Disturbance and Primate-Parasite Dynamics
The direct pathological effects and accompanying reduction in host condition
resulting from parasitic infections may play a role in the lower abundance and species
richness of primate communities in disturbed systems. While reproductively active
primate groups may be sustained in forest fragments and selectively logged forests, little
is known about the effects of such disturbance on primate health. These disturbance
regimes result in changes in forest structure and climate, increased human presence, and
decreased food availability (Kapos 1989; Williams-Linera 1990; Laurance et al. 1996;
Didham and Lawton 1999; Chapman et al. 2000; Chapman and Peres 2001). Such
changes may increase or decrease the likelihood of parasite infection. Forest fragments
have consistently lower canopy height and higher foliage density than continuous forest

7
(Williams-Linera 1990; Camargo 1993; Malcolm 1994; Laurance et al. 1996). Higher
foliage density has also been demonstrated for selectively logged forests (Ganzhom
1995). Lower canopy height may increase overlap in arboreal pathways among primates
and higher foliage density may increase the surface area exposed to falling feces.
Consequently, these characters may increase the probability of contact with infected fecal
material for primates. However, microclimatic change resulting from disturbance may
negatively influence the lifecycle of a parasite (Stuart et al. 1993). Forest fragments
maintain higher temperature and higher rates of evaporative drying compared to
continuous forest (Kapos 1989; Laurance et al. 1996; Didham and Lawton 1999). Such
abiotic conditions may result in shorter survival time for free-living larvae within fecal
material because of rapid desiccation (Meade 1983).
Forest fragmentation and selective logging are often accompanied by increased
contact between primates and humans. Primates act as reservoirs for human pathogens
and likewise, humans act as reservoirs for diseases to which other primates are
susceptible (Lopez-Neyra 1949; Brown and Neva 1983; Meade 1983; Horii and Usui
1985; Stuart et al. 1990; Wolfe et al. 1998). With increased population densities of
humans and inflated densities of primates in fragmented habitats, the probability of
contact with infectious fecal material and infected hosts increases. Thus, increased
contact with humans may increase infection risk for primates in forest fragments and
selectively logged forests.
In forest fragments, primate densities may be high because of immigration from
cleared areas (Onderdonk and Chapman 2000). Thus, groups there often have more
restricted, overlapping ranges than do groups in continuous forest. Crowding and re-use

8
of restricted areas may increase the probability of a primate coming into contact with an
infected individual or areas contaminated with infectious fecal material. For example,
chimpanzees (Pan troglodytes) and howling monkeys (Alouatta palliata and A.
seniculus) demonstrate higher prevalence of parasite infections in groups with restricted
ranges or in groups at higher population density (McGrew et al. 1989; Stuart et al. 1990;
Gilbert 1994). Gilbert (1994) also demonstrated that prevalence of endoparasitic
infection was positively correlated with the density of sympatric primate species. Thus,
crowding resulting from forest fragmentation may increase transmission of infectious
parasites among primates.
If there is a reduction of food availability associated with forest fragmentation or
selective logging, this may result in decreased animal condition. Reductions in animal
condition due to food stress can increase vulnerability to disease or parasites, resulting in
population declines (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). Thus,
it appears likely that human disturbance, such as forest fragmentation and high-intensity,
selective logging may alter the risk of parasite infection for primates.
Rationale
My objective was to determine the consequences of various forms of human
disturbance (including selective logging and forest fragmentation) on primate-parasite
dynamics. To meet this objective, I intensively surveyed the primate community of
Kibale National Park and surrounding areas to determine prevalence and diversity of
gastrointestinal parasites. Chapter 2 presents the findings of these surveys for the guenon
species. Chapter 3 presents the findings of these surveys for the colobine species. Next,
I compared infection dynamics for red colobus, black-and-white colobus, and redtail
guenons between selectively logged forest and undisturbed forest. Details of this aspect

9
of the study are presented in Chapter 4. I made a similar comparison, examining
infection dynamics for red colobus and black-and-white colobus between forest
fragments and undisturbed forest. Details of this aspect of the study are presented in
Chapter 5. Finally, I examined the relationship among physical and biological attributes
of forest fragments and strongyle nematode infection dynamics in red colobus. Details of
this aspect of the study are presented in Chapter 6.

CHAPTER 2
GASTROINTESTINAL PARASITES OF THE GUENONS OF WESTERN UGANDA
Introduction
The guenons, Cercopithecus spp., are the most diverse taxa of primates endemic to
sub-Saharan Africa (Grubb et al. 2002). These frugivorous monkeys live in groups of 10-
30 individuals and often form mixed-species associations with other primate species
(Chapman and Chapman 2000). Although guenons can be found in a wide variety of
habitats, the majority inhabit tropical forests (Butynski 2002). More than two-thirds of
sub-Saharan Africas original forest cover has been lost because of anthropogenic
disturbance (World Resources Institute 1998), and forest cover continues to decline at a
rate of 0.7% annually (FAO 1999). Due largely to resultant habitat loss, 26% of guenons
are endangered (Butynski 2002).
Although parasite infections are common in nature and low-intensity infections are
often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic
change may result in a loss of stability associated with altered transmission rates, host
range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline
data on patterns of parasitic infections in wild guenon populations are critical to provide
an index of population health, and to begin to assess and manage disease risks.
Although many studies have documented the gastrointestinal parasites of wild
populations of African apes (Huffman et al. 1997; Graczyk et al. 1999; Nizeyi et al. 1999;
Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et al.
1989; Miiller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other
10

11
African primate taxa remain poorly known. The present study identifies and quantifies
the gastrointestinal helminth parasites for the 4 guenon species of western Uganda: redtail
guenons (Cercopithecus ascanius), blue monkeys (C. mitis), l'hoesti monkeys (C.
Ihoesti), and vervet monkeys (C. aethiops). For the most common species (the redtail
guenon), I also report protozoan parasites, and examine the effect of season and host sex
on parasite prevalence.
Materials and Methods
From January 1998 to December 2002,1 collected 293 fecal samples from free-
ranging guenons at forested sites in western Uganda; 235 from redtail guenons, 35 from
blue monkeys, 11 from l'hoesti monkeys, and 12 from vervet monkeys. Samples from
redtail guenons, blue monkeys, and lhoesti monkeys were collected in Kanyawara, a
1,034 ha area characterized by logged and unlogged forest within Kibale National Park
(766 km2; 013'-04r N, 3019'-3032' E; Struhsaker 1997). Samples from vervet
monkeys were collected at Lake Saka, a forest fragment 30 km northwest of the national
park. The region experiences a bimodal pattern of seasonal rainfall, with peaks occurring
in March-May and August-November (Figure 2-1). Mean annual rainfall (1990-2001) is
1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged
14.9C and 20.2C, respectively, from 1990 to 2001.
Samples were collected immediately after defecation to avoid contamination, and
were examined microscopically for adult nematodes and tapeworm proglottids. With the
exception of redtail guenons, samples represent individuals. In the case of redtail
guenons, samples are the result of repeated collections from approximately 150 animals.
Samples were stored individually in 5.0-mL sterile vials in 10% neutral formalin solution.
Preserved samples were transported to the University of Florida, where they were

12
examined for helminth eggs and larvae, and protozoan cysts, using concentration by
sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Parasites were
identified on the basis of egg or cyst color, shape, contents, and size. Iodine was used to
facilitate protozoan identification. Measurements were made to the nearest 0.1 p SD,
using an ocular micrometer fitted to a compound microscope; and representatives were
photographed. Mean egg sizes presented are based on measurement of 10 eggs from 10
different hosts unless otherwise noted. Coprocultures (10 per guenon species except
vervets), were used to match parasite eggs to larvae for positive identification of
strongylate nematodes (MAFF 1979). Our capacity to identify most parasite species
from host fecal examination, even with cultured larvae, is limited. Thus, I present most
of my findings at the level of family or genus.
I performed chi-square tests of independence to compare the prevalence of
infections between redtail guenons and blue monkeys. Small sample size precluded me
from including l'hoesti and vervet monkeys in these comparisons. Chi-square tests of
independence were also performed to compare prevalence between host sex for redtail
guenons, and to compare prevalence for the blue monkey population to previously
published reports. I used Pearson correlations to test for relationships between monthly
rainfall and prevalence of parasites infecting redtail guenons.
Results
Nematoda
Trichuroidea: Trichuris sp. was identified based on egg size and morphology
(barrel-shape, yellow-brown coloration, and bipolar plugs). Eggs were found in feces of
all guenon species, and measured 55.1 1.2 X 27.2 1.1 pm for redtail guenons, 60.0
2.0 X 27.0 1.4 pm for blue monkeys, 58.3 1.2 X 27.1 1.1 pm for l'hoesti monkeys,

13
and 57.9 1.4 X 26.7 1.6 pm for vervets. Prevalence of infection with Trichuris sp.
did not differ between redtail guenons (30%) and blue monkeys (26%) (P > 0.05, Table
2-1).
Strongyloidea: Oesophagostomum sp. was identified on the basis of egg size and
morphology (elliptical, unlarvated) and cultured larvae. Eggs were found in feces of all
guenon species except vervets, and measured 69.1 1.8 X 42.4 2.0 pm for redtail
guenons, 70.5 2.0 X 41.3 1.7 pm for blue monkeys, and 73.1 1.2 X 43.0 1.4 pm
for l'hoesti monkeys. Prevalence of Oesophagostomum sp. did not differ (P > 0.05)
between redtail guenons (10%) and blue monkeys (9%) (Table 2-1). Unidentified
strongyle eggs were found in vervet feces (42%) and measured 72-52 X 42-35 pm.
These strongyles may represent Nectator sp., Ancylostoma sp., and/or Oesophagostomum
sp.; however, coprocultures were not performed, limiting our ability to identify these
parasites.
Rhabditoidea: Strongyloides fulleborni was identified based on egg size and
morphology (oval, thin-shelled, colorless, larvated) and verified by cultured rhabditiform
larvae. Eggs were found in feces of all guenon species, and measured 50.2 2.3 X 33.7
4.1 pm for redtail guenons, 43.7 5.0 X 35.4 3.1 pm for blue monkeys, 46.5 3.4 X
34.6 2.3 pm for l'hoesti monkeys, and 47.1 3.7 X 34.4 2.6 pm for vervets.
Prevalence of infection with S. fulleborni did not differ between redtail guenons (7%) and
blue monkeys (6%) (P > 0.05, Table 2-1).
Oxyuroidea: Eggs that appear to be Enterobius sp. based on egg size and
morphology were found in 2 redtail guenon samples (Table 2-1), and measured 64-66 X
36-37 pm (n = 2). This parasite is more reliably diagnosed by examination of peri-anal

14
skin or by necropsy (Ashford et al. 2000). Consequently, these prevalence values may be
underestimations of actual prevalence.
Spiruroidea: Eggs that most closely resemble Streptopharagus sp. (symmetrical,
larvated, thick-shelled) were found in feces of all guenon species, except lhoesti
monkeys, and measured 38.5 2.1 X 24.3 1.1 pm for redtail guenons, 40.1 1.9 X
25.0 1.3 pm for blue monkeys, and 41.7 1.8 X 25.6 1.5 pm for vervets. Prevalence
of Streptopharagus sp. did not differ (P > 0.05) between redtail guenons (18%) and blue
monkeys (14%) (P > 0.05, Table 2-1).
Cestoda
Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed
oncosphere) were found in feces of only 1 redtail guenon, and measured 40-43 X 48-51
pm (n = 4); and no proglottids were detected through macroscopic inspection of feces
(Table 2-1). Since eggs of this species are passed in proglottids, they are not mixed
heterogeneously in feces. Consequently, these prevalence values may be gross
underestimations of actual prevalence.
Trematoda
A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,
operculated, golden-brown coloration). Eggs were found in feces of all guenon species
except lhoesti monkeys, and measured 45.8 1.1 X 24.2 1.0 pm for redtail guenons,
44 X 24 pm for blue monkeys, and 46 X 24 pm for vervets. Prevalence of this trematode
did not differ (P > 0.05) between redtail guenons (2%) and blue monkeys (3%) (Table 2-
1)-

15
Protozoa
Cysts of 3 amoebae and 2 flagellates were identified from 235 fecal samples from
redtail guenons. Cysts most closely resembling Entamoeba coli were multinucleate, with
a mean diameter of 17.8 1.1 pm. Cysts most closely resembling Entamoeba histolytica
had a mean diameter of 12.9 2.1. Cysts most closely resembling Iodameoba butschlii
had a single nucleus, distinct glycogen vacuole, and a mean diameter of 11.2 2.1. Cysts
most closely resembling Giardia lamblia were ovoid with a mean diameter of 11.4 1.4.
Cysts most closely resembling Chilomastix mesnili were lemon-shaped, with a mean
diameter of 7.5 1.1. Prevalence in redtail guenons was relatively low for all
protozoans; Entamoeba coli (11%), Entamoeba histolytica (10%), Iodameoba butschlii
(10%), Giardia lamblia (4%), and Chilomastix mesnili (1%).
Effect of Season and Host Sex on Infection Prevalence
While prevalence did not correlate with monthly rainfall for any parasite species
infecting redtail guenons (P > 0.496), seasonal fluctuations did occur (Figure 2-1).
Although prevalence did not differ between male (n = 12) and female (n = 98) redtail
guenons for any shared parasite species (P > 0.05), Oesophagostomum sp. (n = 24) and S.
fulleborni (n = 16) infections were only detected in adult females.
Variation in Prevalence among Sites throughout Africa
Previous studies have investigated the gastrointestinal parasites of blue monkeys
from South Africa (Appleton et al. 1994) and Kenya (Munene et al. 1998). Comparisons
with my study demonstrate great similarity in helminth faunas of blue monkeys among
sites. However, prevalence varied greatly among sites. Trichuris sp. prevalence was
lower in blue monkeys in Uganda compared to those in Kenya and South Africa (X2 =
11.96, P < 0.005). Prevalence of Oesophagostomum sp. in blue monkeys was higher in

16
Kenya than in Uganda, and higher in Uganda than in South Africa (X2 = 64.03, P <
0.001). Strongyloides sp. prevalence was higher in blue monkeys in Kenya compared to
those in Uganda and South Africa (X2 = 93.85, P < 0.001). Prevalence of
Streptopharagus sp. in blue monkeys was higher in South Africa than in Kenya, and
prevalence in Kenya was higher than in Uganda (X2 = 54.66, P < 0.001). Infections of an
anoplocephalid, thought to be Bertiella sp., were documented for blue monkeys in South
Africa and Uganda and prevalence was higher in blue monkeys in South Africa compared
to those in Uganda (X2 = 32.35, P < 0.001).
McGrew et al. (1989) reported on the gastrointestinal parasites of vervet monkeys
in Senegal. Although Trichuris sp. infections were not documented, and another
spiruroid nematode, Physaloptera sp., replaced Streptopharagus sp.; the overall helminth
fauna was similar to that of vervets in my study.
Discussion
To my knowledge, this is the first report of gastrointestinal helminth parasites from
wild populations of redtail guenons and l'hoesti monkeys, and the first report of
gastrointestinal helminth parasites from blue and vervet monkeys from Uganda.
The similarities in gastrointestinal parasite faunas among the guenons of western
Uganda suggest that generalist parasites predominate, supporting the contention that in
communities comprised of closely related species (i.e., Cercopithecus spp.), cross-species
interaction may be an important source of infection risk (Ezenwa 2003). This may be one
reason why redtail guenons associate with unrelated red colobus monkeys far more than
with other guenon species (Chapman and Chapman 2000).
Seasonal patterns of infection were not readily apparent for any of the parasite
species infecting redtail guenons. This result is unexpected, as previous studies of

17
primate parasite infections from tropical forest sites have documented an increase in
prevalence during the rainy season (Freeland 1977; Huffman et al. 1997). It is difficult to
ascertain why seasonal differences were not seen in this study. However, fluctuation in
infection prevalence was high, warranting future investigation of the mechanism behind
these differences (Figure 2-1).
Although no differences in prevalence of infection were apparent between male and
female guenons for shared parasite species, only adult females were infected with
Oesophagostomum sp. and S. fulleborni. This may reflect energy and nutrient stress
associated with producing and raising infants, which may result in an increased
susceptibility to infection (Gulland 1992; Milton 1996).
Studies investigating the gastrointestinal parasites of blue monkeys, revealed
similar helminth faunas among sites (Appleton et al. 1994; Munene et al. 1998). This
might be expected because of the recent origin of blue monkeys (Leakey 1988; Ruvolo
1988). However, parasite prevalence varied greatly among sites. In general, helminth
prevalence was highest for Kenyan blue monkeys (with the exception of Streptopharagus
sp., which had the highest prevalence for South African blue monkeys). In most cases,
intermediate prevalence was seen in Ugandan compared to Kenyan and South African
blue monkeys. Kenyan forests are small and fragmented, compared to those sampled in
Uganda and South Africa (Appleton et al. 1994); and evidence presented in later chapters
of this dissertation suggests that primates living in forest fragments may be more
susceptible to infection, and demonstrate higher prevalence compared to conspecifics
inhabiting large, undisturbed forests. This may explain the high prevalence of infection
in Kenyan blue monkeys compared to the other 2 sites.

18
The helminth fauna of vervets was similar between Uganda and Senegal (McGrew
et al. 1989). However, small sample size precluded comparisons of prevalence.
Freeland (1977) reported on the protozoan parasites of several primate species in
Kibale National Park. His study identified 2 protozoans from redtail guenons not found
in our study (i.e., Entamoeba hartmanni and an unidentified flagellate). Although
Freeland (1977) does identify Chilomastix mesnili cysts from several species, they were
not identified from redtail guenons. Despite these differences, the overall protozoan
fauna of redtail guenons reported by Freeland (1977) and my study were similar.
Unfortunately, Freeland (1977) does not provide data on prevalence.
My study contributes baseline data on the patterns of parasitic infection in wild
guenons, providing a first step toward an index of population health and disease risk
assessment for conservation and management plans of threatened guenon populations.
My study also reveals that many of the gastrointestinal parasites of the guenon species
examined may be zoonotic. Accordingly, future studies are needed to determine risks of
cross-transmission. Mechanisms to reduce such risks would promote human health,
livestock production, and local support for conservation.
Gastrointestinal parasite classification by fecal analyses is weak by its very nature.
However it is the only responsible method to approach threatened species. Future studies
employing molecular analyses and opportunistic necropsies are needed to improve our
classification of the gastrointestinal parasites of guenons, and to improve our
understanding of the risks of epizootic and zoonotic transmission.

Table 2-1. Prevalence (%) of gastrointestinal helminth parasite infections in guenons of western Uganda
Parastie Species
Redtail (n = 235)
Blue (n = 35)
Lhoiste (n = 11)
Vervet (n = 12)
Strongyloides fulleborni
7
6
27
42
Oesophagostomum sp.
10
9
9
0
Unidentified Strongyle
0
0
0
42
Trichuris sp.
29
26
36
58
Streptopharagus sp.
18
14
0
17
Enterobius sp.
1
0
0
0
Bertiella sp.
< 1
0
0
0
Dicrocoeliidae sp.
2
3
0
8
Overall
49
37
55
92

300
250
200
150
100
50
0
Month
Figure 2-1. Inter-monthly variation in parasite infection prevalence of redtail guenons and rainfall at Kibale National Park, Uganda
Rainfall (mm)

CHAPTER 3
GASTROINTESTINAL PARASITES OF THE COLOBUS MONKEYS OF UGANDA
Introduction
Colobinae is a large subfamily of leaf-eating, old-world monkeys represented in
Africa by two genera, Colobus and Piliocolobus (Grubb et al. 2002). These folivorous
monkeys live in groups of highly variable size (5-300 individuals) and often form mixed-
species associations with other primates (Struhsaker 1981; Oates 1994; Chapman and
Chapman 2000). Colobus species are forest-dependent, and consequently, acutely
threatened by human activities that reduce forest cover. More than two-thirds of Sub-
Saharan Africas original forest cover has been lost due to anthropogenic disturbance
(World Resources Institute 1998), and forest cover continues to decline at a rate of 0.7%
annually (FAO 1999). Due largely to this habitat loss, 50% of African colobine species
are endangered and an additional 20% are rare (Grubb et al. 2002).
Although parasite infections are common in nature and low-intensity infections are
often asymptomatic (Anderson and May 1979; May and Anderson 1979), anthropogenic
change may result in a loss of stability associated with altered transmission rates, host
range, and virulence (Daszak et al. 2000; Patz et al. 2000). Within this context, baseline
data on patterns of parasitic infections in wild colobine populations are critical to provide
an index of population health and to begin to assess and manage disease risks.
Although many studies have documented the gastrointestinal parasites of wild
populations of African apes (Huffman et al. 1997; Nizeyi et al. 1999; Graczyk et al.,
1999; Ashford et al. 2000; Lilly et al. 2003) and baboons (Appleton et al. 1986; Eley et
21

22
al. 1989; Mller-Graf et al. 1997; Hahn et al. 2003), the gastrointestinal parasites of other
African primate taxa remain poorly known. This study identifies and quantifies the
prevalence of gastrointestinal helminth and protozoan parasites for the three colobus
species of Uganda: the endangered red colobus (Piliocolobus tephroceles), the eastern
black-and-white colobus (Colobus guereza), and the Angolan black-and-white colobus
(Colobus angolensis). Where data are sufficient, I also examine the effect of season and
host sex on parasite prevalence.
Materials and Methods
From August 1997 to July 2003,1 collected 2,103 fecal samples: 1,608 from red
colobus, 476 from eastern black-and-white colobus, and 19 from Angolan black-and-
white colobus. Red colobus and eastern black-and-white colobus samples were collected
in 21 forest fragments in Western Uganda, and at Kanyawara, a 1,034 ha area
characterized by logged and unlogged forest within Kibale National Park (766 km2;
013'-04r N, 30o19'-3032' E; Struhsaker 1997). Mean annual rainfall (1990-2001) is
1,749 mm (Chapman et al. 2002). Daily temperature minima and maxima averaged
14.9C and 20.2C, respectively, from 1990 to 2001. Angolan black-and-white colobus
samples were collected from three forest fragments adjacent to Lake Nabugabo in
Southeastern Uganda (0o20-025' S, 3150'-3156 E). Annual rainfall ranges from 520
to 1,970 mm (Efitre et al. 2001) and daily temperature minima and maxima average
15.2C and 27.2C, respectively (Meteorology Department, Masaka, Uganda). All sites
experience a bimodal pattern of seasonal rainfall, with peaks occurring in March-May
and August-November (Figure 3-1).
Samples were collected immediately after defecation to avoid contamination and
examined macroscopically for adult nematodes and tapeworm proglottids. Samples were

23
stored individually in 5.0-mL sterile vials in 10% formalin solution. Preserved samples
were transported to the University of Florida where they were examined for helminth
eggs and larvae and protozoan cysts using concentration by sodium nitrate flotation and
fecal sedimentation (Sloss et al. 1994). Parasites were identified on the basis of egg or
cyst color, shape, contents, and size. Iodine was used to facilitate protozoan
identification. Measurements were made to the nearest 0.1 micron SD using an ocular
micrometer fitted to a compound microscope, and representatives were photographed.
Coprocultures and necropsies (MAFF 1979) were used to match parasite eggs to larvae or
adults for positive identification.
I performed chi-square tests of independence to compare the prevalence of
infections between colobus species and between host age and sex classes for a subset of
red colobus (n = 401). Pearson correlation was used to test relationships between
monthly rainfall and prevalence of parasites infecting red colobus and black-and-white
colobus.
Results
Nematoda
Superfamily Trichuroidea: Trichuris sp. was identified based on egg size and
morphology (barrel-shape, yellow-brown coloration, and bipolar plugs) and verified by
adults obtained by necropsy. Eggs were found in feces of all colobus species, and
measured 57.3 1.0 X 27.0 1.3 pm for red colobus, 58.2 1.6 X 26.9 1.2 pm for
eastern black-and-white colobus, and 58.8 1.2 X 27.2 1.4 pm for Angolan black-and-
white colobus. Prevalence of T. trichiura was higher in Angolan black-and-white
colobus than eastern black-and-white colobus (X2 = 5.28, d.f. = 1, P < 0.025, Table 3-1),
and red colobus (X2 = 32.95, d.f. = 1, P < 0.001, Table 3-1). Prevalence T trichiura was

24
higher in eastern black-and-white colobus than red colobus (X2 = 249.94, d.f. = 1, P <
0.001, Table 3-1).
Superfamily Strongyloidea: Oesophagostomum sp. was identified on the basis of
egg size and morphology (elliptical and unlarvated) and verified by cultured larvae and
adults obtained by necropsy. Eggs were found in feces of all colobus species except
Angolan black-and-white colobus, and measured 70.0 1.4 X 41.8 1.6 pm for red
colobus and 70.2 1.8 X 41.6 1.6 pm for eastern black-and-white colobus. Prevalence
of Oesophagostomum sp. was higher in eastern black-and-white colobus than in red
colobus (X2 11.40, d.f. = 1, P < 0.001, Table 3-1).
Unidentified strongyle eggs were found in feces of all colobus species and
measured 59.6 5.6 X 38.2 4.1 pm for red colobus, 63.7 4.8 X 40.1 4.5 pm for
eastern black-and-white colobus, and 68.4 2.0 X 40.3 2.3 pm for Angolan black-and-
white colobus. These strongyles may represent Necator sp., Ancylostoma sp., and/or
Oesophagostomum sp.; however coprocultures were not performed, limiting our ability to
identify these parasites to genus level. Prevalence of unidentified strongyles was higher
for Angolan black-and-white colobus than for either red colobus (X2 = 9.18, d.f. = 1, P <
0.005, Table 3-1) or eastern black-and-white (X2 = 11.87, d.f. = 1, P < 0.001, Table 3-1).
Superfamily Rhabditoidea: Strongyloides fulleborni was identified based on egg
size and morphology (oval, thin-shelled, colorless, and larvated) and verified by cultured
rhabditiform larvae. Eggs were found in feces of all colobus species, and measured 45.7
1.7 X 34.8 2.0 pm for red colobus, 46.7 2.2 X 35.2 2.2 pm for eastern black-and-
white colobus, and 47.0 1.8 X 35.4 2.0 pm for Angolan black-and-white colobus.
Prevalence of S. fulleborni did not differ among colobus species (P > 0.1, Table 3-1).

25
Strongyloides stercoralis was identified based on larvae size and morphology
(rhabditiform esophagus, prominent genital primordium, and short buccal cavity).
Strongyloides stercoralis larvae were found only in the feces of red colobus, and
measured 242.4 4.5 pm in length.
Superfamily Ascaroidea: Ascaris sp. was identified based on egg size and
morphology (round or oval, thick-shelled, brown or yellow brown, and mammillated
albuminous covering). Eggs were found in feces of red colobus and eastern black-and-
white colobus, and measured 65.2 1.3 X 55.8 1.1 pm and 63.9 1.4 X 54.4 1.0 pm,
respectively. Prevalence of Ascaris sp. was higher for eastern black-and-white colobus
than for red colobus (X2 = 10.71, d.f. = 1, P < 0.005, Table 3-1).
Superfamily Oxyuroidea: Colobenterobius sp. was identified based on egg size
and morphology (elliptical and thick-shelled) from red colobus and eastern black-and-
white colobus and and verified by adults obtained by necropsy. Colobenterobius sp. eggs
were found in the feces of red colobus and eastern black-and-white colobus, and
measured 64.8 1.6 X 36.4 1.4 pm and 65.3 1.2 X 36.6 1.6 pm, respectively.
Prevalence of Colobenterobius sp. did not differ between colobus species (P > 0.1, Table
3-1). This parasite is more reliably diagnosed by examination of peri-anal skin or by
necropsy (Ashford et al. 2000). Consequently, these prevalence values are likely an
underestimation of prevalence.
Cestoda
Eggs that most closely resemble Bertiella sp. (spherical, colorless, fully developed
oncosphere) were found in feces of red colobus and eastern black-and-white colobus, and
measured 40.3 0.8 X 48.8 1.2 pm and 41.2 1.4 X 50.0 1.0 pm respectively. No
proglottids were detected through macroscopic inspection of feces. Prevalence of

26
Bertiella sp. did not differ between colobus species (P > 0.1, Table 3-1). Since eggs of
this species are passed in proglottids, they are not mixed heterogeneously in feces.
Consequently, these prevalence values are likely an underestimation of prevalence.
Trematoda
A dicrocoeliid liver fluke was identified based on egg morphology (ellipsoid,
operculated, golden-brown coloration). Eggs were found in feces of red colobus (46 X
24 pm) and eastern black-and-white colobus (43.8 1.1 X 23.6 1.4 pm). Prevalence of
Dicrocoelium sp. was higher for eastern black-and-white colobus than red colobus (X =
5.34, d.f. = 1, P< 0.025, Table 3-1).
Protozoa
Multinucleate cysts most closely resembling Entamoeba coli were found in the
feces of all colobus species and had a mean diameter of 18.1 1.0 pm for red colobus,
17.4 1.4 pm for eastern black-and-white colobus, and 17.6 1.3 pm for Angolan black-
and-white colobus. Prevalence of E. coli was higher for eastern black-and-white colobus
than red colobus (X2 = 4.28, d.f. = 1, P< 0.05, Table 3-1).
Cysts most closely resembling Entamoeba histolytica were found in the feces of all
colobine species and had a mean diameter of 13.2 1.1 pm for red colobus, 12.5 1.8
pm for eastern black-and-white colobus, and 12.7 1.6 pm for Angolan black-and-white
colobus. Prevalence of E. histolytica was higher for eastern black-and-white colobus
than red colobus (X2 = 14.68, d.f. = 1, P< 0.001, Table 3-1).
Ovoid cysts most closely resembling Giardia lamblia were only found in the feces
of red colobus and had a mean diameter of 11.9 1.8 pm (Table 3-1).

27
Effect of Season and Host Sex on Infection Prevalence
While prevalence did not correlate significantly with monthly rainfall for any
parasite species infecting red colobus (P > 0.077) or eastern black-and-white colobus (P
> 0.081), variation over the year was evident (Figure 3-1).
Prevalence of S. fulleborni was higher in adult male red colobus compared to adult
females (X2 = 6.19, d.f. = 2, P < 0 .05). However, prevalence did not differ for any other
shared parasite species between age and sex classes (P > 0.05).
Discussion
To my knowledge, this is the first report of gastrointestinal parasites from wild
populations of colobus monkeys. The similarities in gastrointestinal parasite faunas
among the colobus of Uganda demonstrate that generalist parasites predominate. This
supports the suggestion that in communities comprised of closely related species, cross
species interaction may be an important source of infection risk (Ezenwa 2003). This
may be one reason that colobines associate with unrelated guenons far more than with
other colobus species (Chapman and Chapman 2000). It is also important to note that
many of the species infecting colobines in Uganda occur at high frequency in the human
populations in the region (NEMA 1997). Consequently, zoonotic and/or
anthropozoonotic transmission may occur and may be promoted by various forms of
anthropogenic disturbance.
Despite the great correspondence in parasite faunas among colobines, prevalence
varied greatly with red colobus having the lowest prevalence and Angolan black-and-
white colobus having the highest prevalence. Prevalence is likely affected by complex
interactions among environmental, demographic, genetic, and behavioral factors, making
it difficult to explain this variation in prevalence. However, one relationship is

28
noteworthy. Unlike red colobus, eastern black-and-white colobus are known to descend
into swampy areas to feed on aquatic vegetation (Oates 1978) where incidental ingestion
of intermediate host or encysted trematodes is likely. Also, eastern black-and-white
colobus are known to come to the group to eat soil and charcoal, much more frequently
than red colobus (Gillespie pers. obs.). This may explain the higher prevalence of the
dicrocoeliid liver fluke in eastern black-and-white colobus than red colobus.
Seasonal patterns of infection were not readily apparent for any of the parasite
species infecting red colobus or eastern black-and-white colobus. This result is
unexpected, as previous studies of parasite infections from tropical forest frugivorous
monkeys and apes have documented an increase in prevalence during the rainy season
(Lophocebus albigena Freeland 1977; Pan troglodytes Huffman et al. 1997). It is
difficult to determine why seasonal differences were not seen in these folivores.
However, variation in infection prevalence was evident over the year, warranting future
investigation of the mechanism behind these differences (Figure 3-1).
Prevalence of S. fulleborni was higher in adult male compared to adult female red
colobus. Perhaps this reflects energy and nutrient stress associated with maintaining
social dominance (Hausfater and Watson 1976), which may result in an increased
susceptibility to infection (Gulland 1992; Milton 1996). However, if this is the case, it is
not clear why infection prevalence is not higher for other parasite species in males
compared to females.
Freeland (1977) provided a survey of the protozoan parasites of primate species in
Kibale National Park that failed to document the presence of any protozoan in colobus
feces based on examination of a small number of samples for red colobus (n = 5) and

29
eastern black-and-white colobus (n = 7). This differs from my results, which demonstrate
that colobines are susceptible to protozoan infection. However, my results reveal that
protozoan prevalence for colobines is low compared to other primate species examined
by Freeland (1977) (e.g., chimpanzees, baboons). Accordingly, it is likely that greater
sampling effort during this earlier study would have yielded findings similar to my own.
This study contributes baseline data on the patterns of parasitic infection in wild
colobus monkeys, providing a first step toward an index of population health and disease
risk assessment for conservation and management plans of threatened and endangered
colobus populations. I documented that the vast majority of gastrointestinal parasites of
wild colobus may be zoonotic or anthropozoonotic. Accordingly, future studies are
needed to determine risks of cross-transmission. Mechanisms to reduce such risks may
promote human health, livestock production, and local support for conservation.
Gastrointestinal parasite classification by fecal analyses is weak by its very nature.
However it is the only responsible method to approach threatened species. Future studies
employing molecular analyses and opportunistic necropsies are needed to improve our
classification of the gastrointestinal parasites of guenons, as well as to improve our
understanding of the risks of epizootic and zoonotic transmission.

Table 3-1. Prevalence (%) of gastrointestinal helminth parasite infections in colobus monkeys of Uganda
Parasite Species Piliocolobus tephroceles in = 1,608)
Colobus suereza in = 476)
Colobus ansolensis in =19)
Strongyloides fulleborni
4
4
5
Strongyloides stercoralis
< 1
0
0
Oesophagostomum sp.
3
6
0
Unidentified strongyle
2
1
11
Asear is sp.
< 1
1
0
Trichuris trichiura
38
79
1
Colobenterobius sp.
< 1
1
0
Bertiella sp.
< 1
< 1
0
Dicrocoelium sp.
< 1
1
0
Entamoeba coli
4
8
16
Entamoeba histolytica
3
8
11
Giardia lamblia
1
0
0
Overall
38
79
100

Rainfall (mm)
31
Figure 3-1. Inter-monthly variation in parasite infection prevalence of colobus monkeys
and rainfall at Kibale National Park, Uganda. A) Red colobus monkeys. B)
Eatem Black-and-white colobus monkeys. (Grey bars represent rainfall.
Black lines represent parasite prevalence).
Prevalence

CHAPTER 4
LONG-TERM EFFECTS OF LOGGING ON PARASITE DYNAMICS IN AFRICAN
PRIMATE POPULATIONS
Introduction
With few areas legally protected from human exploitation, the conservation of
many species will depend on the capacity of disturbed areas to support their populations.
Knowledge of how particular species are affected by specific forms of anthropogenic
environmental change is essential for developing sound conservation and management
plans, as well as assessing the relative conservation value of various disturbed habitats.
Selective logging is a dominant habitat disturbance pattern with strong conservation
potential (Frumhoff 1995; Struhsaker 1997; FAO 1999; Chapman and Peres 2001). A
multitude of studies have examined the effects of selective logging on the abundance and
diversity of invertebrate (Willott et al. 2000; Lewis 2001; Summerville and Crist 2002;
Hamer et al. 2003) and vertebrate taxa (Johns and Skorupa 1987; Johns 1992; Heydon
and Bulloh 1997; Marsden 1998; Robinson and Robinson 1999). Although logging often
results in a reduction in overall diversity, effects on individual species are difficult to
predict. The nature and intensity of response appear to vary depending on species and
site characteristics. For example, following heavy logging at Kibale National Park in
Uganda, red colobus monkeys (Piliocolobus tephroceles) declined, while black-and-
white colobus monkeys (Colobus guereza) increased in density (Chapman et al. 2000).
Another primate, the blue monkey (Cercopithecus mitis) declined after logging at Kibale,
32

33
but increased following similar intensity logging at another site in Uganda (Plumptre and
Reynolds 1994; Chapman et al. 2000).
Ninety percent of primate species are restricted to the tropics, and the majority are
forest dependent (Chapman and Peres 2001). Consequently, with 5 to 6 million ha of
tropical forest selectively logged each year (FAO 1990; FAO 1999), it is not surprising
that primates have been the focus of much research concerning the impact of logging on
biodiversity (Johns and Skorupa 1987; Johns 1997; Struhsaker 1997; Chapman et al.
2000). Although logging is known to negatively impact the abundance of some primate
species, the proximate mechanism for these declines remains unknown. Implied
mechanisms include altered ranging patterns (Johns 1997) and reduced food-tree density
(Skorupa 1988; Struhsaker 1997; Chapman et al. 2000). However, contrasting sites to
arrive at generalities is often difficult, as some areas experience increased hunting
pressure after logging, while others areas do not (Mittermeier 1987; Peres 1990; Oates
1994; Robinson and Bennett 2000). Support for the operation of particular mechanisms
for primate declines following logging is largely indirect and it is unlikely that a single
correlate will explain the complex relationship between primate declines and logging-
induced ecological change. The potential role of parasites and infectious disease in such
primate population declines remains largely unexplored.
Helminthic and protozoal parasites can impact host survival and reproduction
directly through pathological effects and indirectly by reducing host condition (Chandra
and Newbeme 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop
and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous
abortion, congenital malformations, and death (Chandra and Newbeme 1977;

34
Despommier et al. 1995). However, less severe infections are more common and may
impair nutrition, travel, feeding, predator escape, and competition for resources or mates;
or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and
Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate
mechanisms, parasites can potentially regulate host populations (Gregory and Hudson
2000; Hochachka and Dhondt 2000).
Selective logging results in changes in forest structure and food availability
(Skorupa 1988; Ganzhom 1995; Chapman and Chapman 1997; Chapman et al. 2000).
Such changes may alter parasite dynamics in wildlife populations. For example,
Ganzhom (1995) demonstrated that selectively logged forests have higher foliage density
than unlogged forests. Higher foliage density translates to greater surface area exposed to
falling feces and possibly an increased probability of contact with infected fecal material
for arboreal animals. In addition, many forest species are stressed following selective
logging due to reduced food availability. Various forms of environmental stress have
been suggested to increase susceptibility to parasitic infection, and stress and disease are
thought to act synergistically to increase morbidity and mortality (Scott 1988; Holmes
1996; Lafferty and Holt 2003). Reductions in animal condition due to food stress have
been documented to increase vulnerability to infection, and result in lower fertility and
higher mortality (Munger and Karasov 1989; Milton 1996; Murray et al. 1998). In
addition, animal body condition and reproductive status are compromised when parasites
inflict substantial energetic costs (Hudson 1986; Moller 1993; Toque 1993; Rigby and
Moret 2000). However, parasites do not necessarily induce negative effects if hosts have
a sufficient energy or nutrient surplus concurrent with infection (Munger and Karasov

35
1989; Gulland 1992; Milton 1996). This suggests that the outcome of host-parasite
associations may be contingent on host nutritional status as well as severity of infection.
Emerging infectious diseases have raised global awareness of the potential impact
ecological change can have on biodiversity conservation and wildlife and human health
(Meffe 1999; Daszak et al. 2000; Patz et al. 2000; Deem et al. 2001; Lafferty and Gerber
2002). To better develop strategies to deal with established and changing patterns of
disease, we must understand the interplay among alteration and fragmentation of
ecosystems, wildlife-human disease linkages, and the ecology of novel diseases. This
study aims to improve our understanding of this interplay by examining the effects of
selective logging on parasite dynamics in three primate species, the redtail guenon
(Cercopithecus ascanius), the red colobus (Piliocolobus tephroceles), and the black-and-
white colobus (Colobus guereza) in Kibale National Park, Uganda. I compare the
prevalence, diversity, and mean number of gastrointestinal parasite species infecting
individuals, and the relative infection risk between primates from logged and undisturbed
forests. My investigation proposes explanations for similarities and differences in
parasite dynamics between logged and undisturbed forests and addresses the implications
of these findings to conservation and management strategies.
Materials and Methods
Study Site
Kibale National Park (766 km2) is located in western Uganda (lat 0 13'-041' N,
long 3019'-3032' E ) near the base of the Ruwenzori Mountains (Struhsaker 1997).
Tall, closed-canopy forest accounts for 57% of the park. The remainder forms a mosaic
of swamp (4%), grasslands (15%), pine plantations (1%), and colonizing forest (19%)
(Chapman and Lambert 2000). The study site, Kanyawara, is located at the northern end

36
of the park at an elevation of 1,500 m (Gillespie and Chapman 2001). Kanyawara
experiences a bimodal pattern of seasonal rainfall, with peaks occurring in March-May
and August-November. Mean annual rainfall (1990-2001) is 1,749 mm (Chapman et al.
2002). Daily temperature minima and maxima averaged 14.9C and 20.2C,
respectively, from 1990 to 2001.
Prior to becoming a National Park in 1993, Kibale was a Forest Reserve, gazetted
in 1932 with the stated goal of providing a sustained production of hardwood timber
(Osmaston 1959). A polycyclic felling cycle of 70 years was initiated, and it was
recommended that logging open the canopy by approximately 50% through the harvest of
trees> 1.52 m in girth (Kingston 1967). This history of logging has led to varying
degrees of disturbance among sites. I conducted my study in two forestry compartments;
one logged at high intensity in the late 1960s (K-15), and one undisturbed (K-30).
The K-15 forestry compartment is a 347-ha section of forest that experienced high-
intensity, selective felling from September 1968 through April 1969. Total harvest
averaged 21 m3/ha or approximately 7.4 stems/ha (Struhsaker 1997), but incidental
damage was much higher. It is estimated that approximately 50% of all trees in
compartment K-15 were destroyed by logging and incidental damage (Skorupa 1988). A
total of 18 tree species were harvested, with nine species contributing more than 95% of
the harvest volume (Kasenene 1987; Skorupa 1988). Many of the tree species harvested
provided primates with food (Struhsaker 1997; Chapman et al. 2000).
The K-30 forestry compartment is a 282-ha area that has not been commercially
harvested. Prior to 1970, however, a few large stems (0.03-0.04 trees/ha) were removed
by pitsawyers. This extremely low level of extraction seems to have had little effect on

37
the structure and composition of the forest (Skorupa and Kasenene 1984; Struhsaker
1997). Hence, compartment K-30 serves as a control plot for my comparisons. As a
control, I assume that differences between the undisturbed compartment and the logged
compartment are due only to the effects of logging. This is not ideal as some differences
could be the result of naturally occurring variation in forest structure. However, these
compartments are in close proximity (< 2 km apart), and there are few marked
differences between them in terms of physical characters that influence forest structure.
The study area has been protected from human exploitation since the 1970s, and
the hunting of primates ceased in the region in the early 1960s (Struhsaker 1997;
Chapman et al. 2000). The site's primates have been studied extensively, with over 30
years of primate research and substantial background information on the majority of
primate species present (Struhsaker 1997; Chapman et al. in press). For these reasons, a
number of primate groups are habituated, encounter rate is high, and long-term data are
available on several groups for most primate species.
Fecal Sampling and Analysis
From August 1997 to August 2002,1 collected 1,076 fecal samples from primates
in forest compartments K-15 and K-30; 157 from red-tail guenons, 231 from black-and-
white colobus, and 688 from red colobus. All samples were collected immediately after
defecation to avoid contamination and examined macroscopically for adult nematodes
and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile vials in a
10% neutral formalin solution. Preserved samples were transported to the University of
Florida where they were examined for helminth eggs and larvae and protozoan cysts
using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994;
Greiner and Courtney 1999). Parasites were counted and identified on the basis of egg or

38
cyst color, shape, contents, and size. Iodine was occasionally used to facilitate protozoan
identification. Measurements were made to the nearest 0.1 micron SD using an ocular
micrometer fitted to a Zeiss compound microscope. Unknown parasites were
photographed for later identification. Coprocultures and necropsies were used to match
parasite eggs to larvae and adult worms for positive identification (MAFF 1979; Greiner
and Courtney 1999). I report data on helminth eggs per gram of feces (EPG) only as an
indication of environmental contamination (i.e., infection risk), as helminth egg
production is highly variable and rarely indicative of actual infection intensity.
Infection Risk Assessment
From January to August 2002,1 conducted a comparative survey to determine an
index of risk of helminth infection to primates inhabiting logged and undisturbed forests.
Canopy vegetation, ground vegetation, and soil plots from logged and unlogged forests
were collected and analyzed to determine the density of infective-stage individuals for the
two parasite species most prevalent in all three primate species, Trichuris sp. (eggs) and
Oespohagostomum sp. (L3 larvae). Twenty-eight 1 m3 vegetation plots were collected at
a height of 12 m from canopy trees used within the previous two hours by red colobus; 14
from logged forest (K-15), and 14 from undisturbed forest (K-30). Access to the canopy
for collection of vegetative plots was facilitated by single rope climbing technique
(Mitchell, 1982; Laman, 1995). An additional 28 1 m3 ground vegetation plots were
collected below all trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches)
were collected within selected ground vegetation plots, 10 from the logged forest and 10
from the unlogged forest. I used a modified sedimentation technique to recover infective-
stage parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using
a modified Baermann method (Sloss et al. 1994). Samples from all plots were examined

39
by dissecting and compound scope. Infective-stage primate parasites were identified and
counted.
Statistical Analyses
I employed chi-square tests of independence to compare the prevalence of infection
between the logged and undisturbed forests for overall and specific infections for each of
the three primate species. Independent sample t-tests were performed to compare the
mean number of parasite species infecting individual primates and the density of
infective-form parasites in vegetative plots between the logged and undisturbed forests
(SPSS, version 10, 1999).
Results
Infection Prevalence and Richness
Descriptions of taxa, mode of infection, and associated pathology for each parasite
species recovered can be found in Table 4-1. The prevalence of infection with Trichuris
sp., Streptopharagus sp., Strongyloid.es fulleborni, Oespohagostomum sp., Entamoeba
coli, E. histolytica, and Iodameoba buetschlii was higher for redtail guenons from logged
forest compared to guenons from undisturbed forest (Table 4-2). Only redtail guenons
from logged forest were infected with Enterobius sp., a dicrocoeliid liver fluke, Bertiella
sp., Giardia lamblia, and Chilomastix mesnili (Table 4-2). There were no species of
parasite found only in undisturbed forest. The mean number of parasite species infecting
individual redtail guenons was greater in logged compared to undisturbed forest (t = 5.74,
P< 0.001, Figure 4-1).
The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum
sp., E. coli, and E. histolytica did not differ between red colobus from logged and
undisturbed forest (Table 4-3). Only red colobus from undisturbed forest were infected

40
with Colobenterobius sp. (Table 4-3). The mean number of parasite species infecting
individual red colobus did not differ between logged and undisturbed forest (t = 1.32, P =
0.186, Figure 4-1).
The prevalence of infection with Trichuris sp., S. fulleborni, Oespohagostomum
sp., the dicrocoeliid liver fluke, E. coli, and E. histolytica did not differ between black-
and-white colobus from logged and undisturbed forest (Table 4-4). Only black-and-white
colobus from logged forest were infected with Colobenterobius sp. and Bertiella sp.
(Table 4-4). The mean number of parasite species infecting individual black-and-white
colobus did not differ between logged and undisturbed forest (t = 0.64, P = 0.524, Figure
4-1).
Infection Risk
Trichuris sp. eggs were more abundant in canopy plots (Disturbed Mean = 1.43
0.20, Undisturbed Mean = 0.47 0.25, t = -2.66, P = 0.013) and ground vegetation plots
(Disturbed Mean = 4.21 0.13, Undisturbed Mean = 0.43 0.96 t = -3.56, P = 0.003)
from logged compared to undisturbed forest. Oesophagostomum sp. L3 larvae were more
abundant in ground vegetation plots from logged compared to undisturbed forest
(Disturbed mean = 3.93 1.23, Undisturbed mean = 0.14 0.11, t= -3.14, P = 0.008), but
were not found in canopy plots. No infective-stage primate parasites were identified
from the soil plots.
Discussion
A recent study demonstrated that group densities for redtail and blue guenons at
Kibale were lower in logged forest than undisturbed forest and that their populations
declined between censuses conducted 12 and 28 years after logging (Chapman et al.
2000). Although Chapman et al. (2000) found red colobus densities to be lower in

41
logged forest than undisturbed forest, their populations were in a state of recovery. In
contrast, the study found black-and-white colobus densities to be higher in logged forest
than in undisturbed forests.
The current study provides insights into the variable responses to logging observed
in these redtail guenon, red colobus, and black-and-white colobus populations. It is clear
that logging at Kibale has altered parasite dynamics resulting in higher densities of
infective-stage parasites common to both guenons and colobines. Despite this higher
infection risk for all three primate species, only redtail guenons manifest higher
prevalence and richness of gastrointestinal parasite infections and a higher mean number
of parasite species infecting individuals in logged compared to undisturbed forests.
These results suggest that guenons are more susceptible to parasitic infection following
selective logging than colobines.
The greater long-term impact of logging on guenon compared to colobine
populations may be a function of altered parasite dynamics in association with food
availability and animal nutrition and condition. Dietary stress may adversely affect
resistance to parasitic infection by reducing the effectiveness of the immune system
(Crompton 1991, Solomons and Scott 1994, Holmes, 1995, Milton 1996). As a result,
food shortages could result in higher parasite intensity, which in turn could increase
nutritional demands on the host and accentuate the effects of food shortages. Under such
conditions, nutritional status and parasitism could have synergistic effects on the host and
the individual effects of each factor would be amplified when co-occurring (Mihook et al.
1985, Keymer and Dobson 1987, Holmes 1995).

42
There is good evidence that logging has greatly reduced guenon food availability at
Kibale. First, recall that approximately 50% of all trees in logged forests were destroyed
by felling and incidental damage and that trees harvested were disproportionately primate
food trees (Skorupa 1988; Struhsaker 1997). This reduction in food availability
following logging likely accounts for much of the initial declines seen in guenon and red
colobus populations. Second, even 25 years after logging, tree growth rates and tree
density for all size classes were lower, while seedling mortality was higher in the logged
compared to undisturbed forests (Chapman and Chapman 1997). This suggests that
logged forests are regenerating poorly. So why have red colobus started to recover, while
guenons have not in logged forests? Recall that selective logging facilitates higher
foliage density as a result of greater sunlight availability (Ganzhom 1995). This
translates to greater food availability and food quality (e.g., a predominance of young
leaves) for the folivorous colobines. In addition, the tree species that colonize disturbed
areas (i.e., Celt is durandii and Funtumia latifolia) have leaves with a higher protein-to-
fiber ratio (i.e., higher food quality; Milton 1998), a component of leaves important in
determining colobine abundance (Chapman and Chapman 2002). From 1990 to 2000, the
total basal area of both C. durandii and F. latifolia, major food species for both
colobines, increased substantially in the logged forest (Chapman and Chapman, in press).
During this same period, growth rates for both of these tree species were higher in the
logged compared to the undisturbed forests (Chapman and Chapman, in press).
Concurrently, food resources for the frugivorous guenons have not been recovering.
Multiple indices of fruit production demonstrated lower fruit availability in the logged
compared to undisturbed forests even 25 years after logging (Chapman and Chapman

43
1997). In addition, at both 22 and 32 years post-logging, the basal area of trees in logged
forests was less than in undisturbed forests (Chapman and Chapman, in press). Thus, a
primary guenon food resource, mature fruit-bearing trees, were reduced significantly in
density by logging and young trees are not successfully regenerating to replace those lost
to logging. Consequently, it is not surprising that red colobus have begun to recover in
parallel with their food resources; while guenons have not recovered.
Although food availability accounts well for the lack of recovery in guenon
populations in logged forests, it is not clear why populations are declining. However,
nutrition and parasite dynamics may interact to play a role in these declines. Correlations
among elevated parasitism, reduced nutrition, and reduced body condition are well
documented (Mori 1979, Eley et al. 1989; Gulland 1992; Milton 1996); however,
causation remains equivocal. Milton (1996) demonstrated that howler monkey (Alouatta
palliata) mortality was best explained by the interaction of age, physical condition,
dietary stress, and intensity of parasitic bot fly infestations. Similarly, Gulland (1992)
found that the timing of population crashes in Soay sheep (Ovis aries) were strongly
correlated with emaciation, high intensity nematode infections, and signs of protein-
energy malnutrition. Moreover, free-ranging sheep treated with antihelminthics had
lower mortality rates, while experimentally infected sheep fed nutritious diets showed no
sign of malnutrition. Recent evidence from Kibale indicates that dietary stress affects
redtail guenons in logged forests. These guenons have lower intake of crude protein and
the majority of key minerals compared to guenons in undisturbed forests (K. Rode,
personal communication). Such protein deficiencies have been linked to depressed
immune function (Chandra 1983; Bundy and Golden 1987; Koski and Scott 2001). In

44
addition, nutrient content varies more among food items for guenons compared to
colobines at Kibale (K. Rode, personal communication). Thus, variation in nutritional
condition is likely more sensitive to changes in habitat for guenons than for colobines.
Parasite infections are common in nature and low-intensity infections are often
asymptomatic. Endemic stability is common, resulting in coexistence of parasite, vector
(in vector-borne parasites), host, and environment such that clinical disease is rare
(Norval et al 1992). However, anthropogenic change may result in a loss of endemic
stability associated with altered vector dynamics, transmission rates, parasite host range,
and parasite virulence (Deem et al. 2001). Resultant high-intensity infections, as well as
moderate-intensity infections in stressed animals, can result in morbidity and mortality.
Comparisons of parasite prevalence can be a useful indirect indicator that parasites
may be impacting host populations (i.e., population declines correlated to increased
infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting
guenons at higher prevalence in the logged forests have the capacity to cause substantial
pathology and death in primates (Table 4-1). Heavy infections of Oesophogostomum sp.,
Strongyloides sp., and Enterobius sp. are associated with mucosal inflammation,
ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and
Johnsen 1978; Holmes et al. 1980; Harper et al. 1982; Liu et al. 1995; Murata et al.
2002). Even moderate intensities of Oesophogostomum sp. have proven clinically
important in stressed captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For
example, nearly 30% of 70 guenons imported to Italy from Senegal died soon after
arrival from severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial
infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent

45
complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of
all parasites infecting guenons in logged forests at Kibale may contribute to greater
morbidity and mortality in this guenon population compared to the population inhabiting
undisturbed forests.
The magnitude and prevalence of multiple-species infections in individuals can be
another useful indirect indicator that parasites may be impacting host populations.
Multiple-species infections are associated with a greater potential for morbidity and
mortality due to synergistic and competitive interactions occurring between parasite
species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sebelis 1995).
For example, concurrent infections with Heligmosomoides polygurus and Trypanosoma
congolense in mice (Fakae et al. 1994) and Escherichia coli and Ascaris suum in pigs
(Adedeji et al. 1989) result in higher mortality than single infections. Similarly, in
humans, Schistosoma, mansoni has an increased effect on the development of
malnutrition in the presence of T. trichiura (Parraga et al. 1996) and a range of parasites
demonstrate greatly elevated pathogenic effects in the presence of HIV (Gomez et al.
1995; Kaplan et al. 1996). Consequently, the elevated frequency and number of multiple-
species infections observed in guenons in logged forests at Kibale may contribute to
greater morbidity and mortality in this guenon population compared to the population
inhabiting undisturbed forests.
Other dietary differences between guenon and colobine species may also play a role
in the patterns observed. Encounter probabilities for some of the parasites involved
would be expected to differ between guenons and colobines. Bertiella sp., Dicrocoelium
sp. and Streptopharagus sp. have intermediate hosts. Guenons feed on many of these

46
intermediate hosts, which include coleopterans, orthopterans, ants, and land snails, while
colobines do not intentionally feed on insects and other invertebrates. Consequently, if
intermediate hosts are more common in logged forests or more intermediate hosts are
infected in logged forests, guenons may have a higher encounter probability for parasites
with indirect life cycles. However, infections with these parasite species are rarely
associated with disease, thus, they are likely of minor importance in regards to guenon
declines in logged forests (Table 4-1).
This study suggests that redtail guenons are more susceptible to parasitic infection
than colobines following selective logging at Kibale National Park in Uganda. Logging
in Kibale is known to impact these frugivorous guenon populations more than folivorous
colobine populations, and parasite dynamics appear to play a role in these patterns of
response. Consequently, conservation initiatives for guenons, and potentially a wide-
range of frugivorous species, should focus on the preservation of intact forests. However,
extractive management plans that avoid the removal of preferred food species, maintain
arboreal pathways, and reduce infection risk may allow for selective logging without the
loss of frugivorous populations.
Although many recent studies and reviews have focused on the conservation
implications of anthropozoonotic disease transmission to wildlife (Stuart and Strier 1995;
Wallis and Lee 1999; Nizeyi et al. 2001; Graczyk et al. 2002; Woodford et al. 2002), the
potential impact of anthropogenic habitat disturbance on disease dynamics in wild
populations has received far less attention. This study demonstrates that one such
disturbance, selective logging, has the capacity to alter parasite dynamics for some
species. Knowledge of how particular species are affected by various forms of ecological

47
change is essential to promote land-use policy that is compatible with animal and human
health and biodiversity conservation.
Our understanding of how anthropogenic habitat change alters wildlife disease
dynamics is in its infancy. Our comprehension of this interplay will be greatly improved
by future research that investigate how selective logging and other forms of
anthropogenic habitat disturbance affect the rates and patterns of parasite and disease
transmission within and between species. In addition, studies are needed that explore how
nutritional state modulates the effects of parasites and the occurrence of disease in wild
populations. Identifying risk factors for disease transmission will improve the ability of
conservationists to make rational decisions about the risks and benefits of extraction and
management activities.

Table 4-1. Mode of infection, morbidity, and mortality associated with gastrointestinal parasites infecting redtail guenon
(Cercopithecus ascanius), red colobus (Piliocolobus tephroceles), and black-and-white colobus (Colobus guereza) in
logged and undisturbed forests at Kibale National Park, Uganda
Parasite Species
Mode of Infection
Morbidity/Mortality
Sources
Trichuris sp.
Embryonated egg ingested
Typically asymptomatic
Beaver et al. 1984; Baskin 1993
Streptopharagus sp.
Intermediate host ingested
(cockroach, beetle)
Typically asymptomatic
Beaver et al. 1984; Coombs and
Crompton 1991
Strongyloides fulleborni
Larvae ingested, skin
Mucosal inflammation,
McClure and Guilloud 1971;
penetration
ulceration, death
Pampiglione and Ricciardi 1972
Oesophagostomum sp.
Larvae ingested
Severe diarrhea, weight loss,
death
Crestian and Crespeau 1975;
Roperto et al. 1985
Enterobius sp.
Egg ingested
Dysentary, enteritis, ulceration,
death
Liu et al. 1995; Murata et al. 2002
Colobenterobius sp.
Egg ingested
Dysentary, enteritis, ulceration,
death
Hugot 1999
Dicrocoeliid liver fluke
Metacercaria ingested in ant
or on vegetation
Typically asymptomatic
Beaver et al. 1984; Coombs and
Crompton 1991
Bertiella sp.
Cysticercoid ingested in
orbatid mite
Typically asymptomatic
Fiennes 1967; Lloyd 1998
Giardia lamblia
Cyst or trophozoite ingested
Typically asymptomatic,
possibly epizoonotic
Fiennes 1967; Baskin 1993
Entamoeba coli
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984
Entamoeba histolytica
Cyst or trophozoite ingested
Hepatic and gastric amoebiasis,
death
Loomis 1983
Chilomastix mesnili
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984
Iodameoba buetschlii
Cyst or trophozoite ingested
Typically asymptomatic
Beaver et al. 1984

Table 4-2. Prevalence (%) of gastrointestinal parasite infections in redtail guenons (Cercopithecus ascanius) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Logged(n = 235)
Undisturbed (n = 35)
Significance
Trichuris sp.
63
21
***
Streptopharagus sp.
32
13
*
Strongyloides fulleborni
16
4
**
Oesophagostomum sp.
21
3
***
Enterobius sp.
5
0
N.A.
Dicrocoeliid liver fluke
11
0
N.A.
Bertiella sp.
3
0
N.A.
Giardia lamblia
26
0
N.A.
Entamoeba coli
26
5
***
Entamoeba histolytica
26
5
***
Chilomastix mesnili
8
0
N.A.
Iodameoba buetschlii
26
5
***
Overall
92
29
***
* P < 0.05, ** P < 0.01, *** P < 0.001, N.A. no chi-square test performed since one forest type had 0 prevalence

Table 4-3. Prevalence (%) of gastrointestinal parasite infections in red colobus (Piliocolobus tephroceles) from logged and undisturbed
forests in Kibale National Park, Uganda
Parasite Species
Logged(n =127)
Undisturbed (n = 561)
Significance
Trichuris sp.
40
36
N.S.
Strongyloides fulleborni
1
4
N.S.
Oesophagostomum sp.
5
2
N.S.
Colobenterobius sp.
0
1
N.A.
Entamoeba coli
6
3
N.S.
Entamoeba histolytica
6
3
N.S.
Overall
45
37
N.S.
N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence

Table 4-4. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from logged and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Logged(n =125)
Undisturbed (n = 106)
Significance
Trichuris sp.
79
84
N.S.
Strongyloides fulleborni
4
3
N.S.
Oesophagostomum sp.
9
9
N.S.
Colobenterobius sp.
2
0
N.A.
Dicrocoeliid liver fluke
1
1
N.S.
Bertiella sp.
1
0
N.A.
Entamoeba coli
16
9
N.S
Entamoeba histolytica
16
9
N.S.
Overall
79
84
N.S.
N.S. P > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence

5
3
O
s:
o
es
a.
-
o
-C
£
s
S3
O
4
3
? -
O
*
Undisturbed
Logged
(n = 38)
(n = 561) (n = 127)
(n = 125)
Redtail Guenon Red Colobus Black-and-White Colobus
Figure 4-1. Mean number of parasite species infecting individual redtail guenon (Cercopithecus ascanius), red colobus (Piliocolobus
tephroceles), and black-and-white colobus (Colobus guereza) in undisturbed and logged forest at Kibale National Park,
Uganda

CHAPTER 5
ALTERED PARASITE DYNAMICS AND PRIMATE POPULATION DECLINES IN
FOREST FRAGMENTS
Introduction
Forest fragmentation reduces overall species diversity and alters species abundance
(Laurance and Bierregaard 1997; Laurance 1999); modifying biological processes such as
predation, competition, and infection dynamics (Crooks and Soule 1999; Terborgh et al.
2001; LoGuidice et al. 2003). To date, empirical evidence has been lacking to test the
relative importance of these factors in explaining the complex relationship between
wildlife declines and fragmentation-induced ecological change. I present support for a
previously unrecognized mechanism for vertebrate declines following forest
fragmentation, altered infection dynamics.
Parasite infections are common in nature and low-intensity infections are often
asymptomatic. Stability is common, resulting in coexistence of parasite, vector, and host
such that clinical disease is unusual (Anderson and May 1979; May and Anderson 1979).
However, anthropogenic change may result in a loss of stability associated with altered
vector dynamics, transmission rates, parasite host range, and parasite virulence (May
1988; Daszak et al. 2000; Patz et al. 2000). Resultant changes in host susceptibility and
infection risk may result in elevated morbidity and mortality, and ultimately, population
declines.
Forest fragmentation results in a suite of alterations that may increase susceptibility
to infection and infection risk in resident populations (Figure 5-1). Environmental
53

54
stressors associated with forest fragmentation, such as reduced food availability and
diversity, density-dependent factors, and more frequent interactions with humans may
reduce immunity and elevate susceptibility to infection (Murray et al. 1998; Lafferty and
Holt 2003). Reduced habitat area following forest fragmentation may result in restricted
ranging and crowding (McCallum and Dobson 2002; Lafferty and Holt 2003), increasing
habitat overlap among conspecifics, thus predisposing individuals to a higher probability
of pathogen contact (Freeland 1977; Altizer 2003). Landscape characteristics of
fragment boundaries influence the frequency and nature of contact among wildlife,
human, and livestock populations, increasing the potential for epizootic and
anthropozoonotic pathogen transmission (Lafferty and Gerber 2002; McCallum and
Dobson 2002).
To improve our understanding of how fragmentation alters infection dynamics, I
quantified gastrointestinal parasites of the endangered red colobus (Piliocolobus
tephroceles) and black-and-white colobus (Colobus guereza) populations in western
Uganda between August 1999 and July 2003. I compare the prevalence, diversity,
number of gastrointestinal parasite species infecting individuals, and relative infection
risk for primates between forest fragments and undisturbed forests within Kibale National
Park. Concurrent censuses of colobus populations allowed us to examine infection
dynamics in relation to host-population dynamics. Our investigation proposes a novel
mechanism for vertebrate declines in forest fragments and addresses implications of these
findings for conservation strategies.

55
Materials and Methods
Study Site
I surveyed 20 forest fragments that lie within the agricultural landscape from the
western boundary of Kibale National Park to the foothills of the Ruwenzori Mountains in
Uganda (013'-04r N, 3019'-3032') (Onderdonk and Chapman 2000). Mean annual
rainfall in the region is 1749 mm (1990-2001) and mean daily minimum and maximum
temperatures are 14.9C and 20.2C, respectively (1990-2001, Chapman and Chapman
unpublished data). Rainfall is bimodal, with two rainy seasons generally occurring from
March to May and September to November.
Prior to agricultural expansion, mid-elevation, moist, evergreen forest dominated
the region (Naughton-Treves 1997). While the precise timing of isolation of these forest
remnants is not known, local elders describe them as 'ancestral forests', and aerial
photographs from 1959 confirm that most have been isolated from Kibale since at least
that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha, are used by
local citizens to varying degrees, and are surrounded by small-scale agriculture or tea
plantations.
I surveyed compartment K-30, a 282-ha area of undisturbed forest situated within
the largely forested Kibale National Park (746 km2)(Struhsaker 1997). Compartment K-
30 is in close proximity to the forest fragments (< 6.5 km apart), and once belonged to the
same tract of forest, minimizing the probability that differences observed are the result of
inherent variation in forest structure and diversity.
Fecal Sampling and Analysis
From August 1999 to July 2003,1 collected 1,151 fecal samples from primates in
20 forest fragments and the K-30 compartment of Kibale National Park: 951 from red

56
colobus and 200 from black-and-white colobus. All samples were collected immediately
after defecation to avoid contamination and examined macroscopically for adult
nematodes and tapeworm proglottids. Samples were stored individually in 5.0 ml sterile
vials in a 10% formalin solution. Preserved samples were transported to the University
of Florida where they were examined for helminth eggs and larvae and protozoan cysts
using concentration by sodium nitrate flotation and fecal sedimentation (Sloss et al.
1994). Parasites were counted and identified on the basis of egg or cyst color, shape,
contents, and size. Iodine was occasionally used to facilitate protozoan identification.
Measurements were made to the nearest 0.1 micron SD using an ocular micrometer
fitted to a compound microscope. Unknown parasites were photographed for later
identification. Coprocultures and necropsies were used to match parasite eggs to larvae
and adult worms for positive identification (MAFF 1979).
Infection Risk Assessment
As an index of infection risk, infective-stage parasite densities were determined for
canopy vegetation, ground vegetation, and soil plots from fragmented and undisturbed
forest. From January to August 2002,1 collected twenty-nine 1 m3 vegetation plots at a
height of 12 m from canopy trees used within the previous 2 hr by red colobus; 15 from
forest fragments and 14 from undisturbed forest. Canopy access for plot collection was
facilitated by single rope climbing technique (Mitchell 1982). An additional 29 1 m3
ground vegetation plots were collected below all trees sampled for canopy plots. Soil
plots (0.05 m3 surface scratches) were collected within randomly selected ground
vegetation plots, 10 from forest fragments and 10 from undisturbed forest. I used a
modified sedimentation technique to recover infective-stage parasites from vegetative
plots (Sloss et al. 1994). Soil plots were examined using a modified Baermann method

57
(Sloss et al. 1994). Samples were examined by dissecting and compound scope, and
infective-stage individuals of the two most prevalent parasite species, Trichuris trichuria
(eggs) and Oespohagostomum stephanostomum (L3 larvae) were counted.
Colobus Surveys
Red colobus and black-and-white colobus populations in forest fragments were
censused from May to August 2000 and recensused May to August 2003. The total
number of colobus in each fragment was counted over 1 to 4 days. Our repeated
censuses of red colobus and black-and-white colobus over the past three decades within
the K-30 compartment of Kibale National Park provide comparable data for these
colobus populations (Chapman et al. 2000).
Statistical Analyses
I employed chi-square tests of independence to compare prevalence between
fragment and undisturbed forest samples for overall and specific infections. Independent
sample t-tests were performed to compare mean number of parasite species infecting
individual primates and density of infective-form parasites in plots between fragmented
and undisturbed forest.
Results
Infection Prevalence and Richness
The prevalence of infection with Trichuris sp., Oespohagostomum sp., Entamoeba
coli, and Entamoeba histolytica was higher for red colobus from forest fragments
compared to red colobus from undisturbed forest, but prevalence did not differ for
Strongyloides fulleborni or Colobenterobius sp. (Table 5-1). Only red colobus from
forest fragments were infected with Strongyloides stercoralis, Ascaris sp., Bertiella sp.,
Giardia lamblia, and unknown strongyles (Table 5-1). There were no species of parasite

58
found only in undisturbed forest. The number of parasite species infecting individual red
colobus was greater in forest fragments compared to undisturbed forest (t = -5.785, P <
0.001, Figure 5-2).
For black-and-white colobus, the prevalence of infection with Trichuris sp., S.
fulleborni, Oespohagostomum sp., a dicrocoeliid liver fluke, E. coli, and E. histolytica did
not differ between animals in forest fragments and undisturbed forest (Table 5-2). Only
black-and-white colobus from forest fragments were infected with Ascaris sp. and
unknown strongyles (Table 5-2). There were no species of parasite found only in
undisturbed forest. The number of parasite species infecting individual black-and-white
colobus did not differ between forest fragments and undisturbed forest (t = -0.219, P =
0.827, Figure 5-2).
Infection Risk
Trichuris sp. eggs were more abundant in canopy plots (fragmented mean = 1.36
0.35 eggs/plot, undisturbed mean = 0.47 0.25 eggs/plot, t = -2.43, P = 0.022) and
ground vegetation plots (fragmented mean = 1.87 0.48 eggs/plot, undisturbed mean =
0.43 0.26 eggs/plot, t = -2.40, P = 0.026) from fragmented compared to undisturbed
forest. Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots
from fragmented compared to undisturbed forest (fragmented mean = 3.33 0.64
larvae/plot, undisturbed mean = 0.14 0.11 larvae/plot, t= -4.95, P < 0.001), but were not
found in canopy plots. No infective-stage primate parasites were identified from the soil
plots.
Colobus Population Dynamics
Ten of the 20 forest fragments censused contained red colobus and persisted for the
duration of the study (i.e., were not cleared). In these fragments, red colobus declined

59
from 163 individuals in 2000 to 131 individuals in 2003, a 20% reduction. Twelve of the
forest fragments censused contained black-and-white colobus and persisted for the
duration of the study. In these fragments, black-and-white colobus increased from 97
individuals in 2000 to 101 individuals in 2003, a 4% increase. Results of red colobus and
black-and-white colobus censuses over the past three decades in the K-30 compartment
of Kibale National Park demonstrate that densities of both colobus species are stable
(Chapman et al 2000).
Discussion
My results demonstrate that forest fragmentation has altered infection dynamics
resulting in higher densities of infective-stage parasites common to red colobus and
black-and-white colobus. Despite this higher infection risk for both species, only red
colobus manifested higher prevalence and richness of gastrointestinal parasite infections
and a higher number of parasite species infecting individuals in fragmented compared to
undisturbed forests. These results suggest that red colobus are more susceptible to
parasitic infection following forest fragmentation than black-and-white colobus.
Reduced food availability and diversity is likely the critical environmental stressor
responsible for this elevated susceptibility of red colobus to infection following forest
fragmentation. Compared to intact forest, fragments have been documented to have
higher rates of tree mortality (Mesquita et al. 1999), increased densities of trees with
wind- or water dispersed seeds, and reduced densities of trees with vertebrate-dispersed
seeds (Tabarelli et al. 1999), of which smaller fruited species predominate (Chapman and
Onderdonk 1998). These trends predict an overall reduction in food resources for
frugivorous and folivorous vertebrates in forest fragments. For species sensitive to
changes in food availability, resultant food stress may increase susceptibility to infection.

60
This appears to be the case for the red colobus. Red colobus typically consume a high
diversity diet (i.e., > 42 species) and their density can be predicted from the abundance of
important food trees (Struhsaker 1975; Chapman et al. 2002). Such broad dietary
requirements might predispose red colobus to food stress in forest fragments, where the
necessary diversity of plant species and parts are not always available (Chapman et al.
2003b). In contrast, black-and-white colobus have a low diversity diet (i.e., < 25 species
with 3 species accounting for 69%) and demonstrate a high degree of dietary flexibility
(Onderdonk and Chapman 2000; Oates 1974). They are clearly capable of persisting on a
monotonous diet dominated by readily available tree species, an advantage for living in
forest fragments with high variation in tree species composition (Chapman et al. 2003b).
However, one population of red colobus has been documented to persist on a very
monotonous diet (Chapman et al. 2002) and as fragments are degraded red colobus are
often the last species to remain. Correlating stress hormones with variation in food
availability and quality would provide insights into whether or not this factor is
responsible for this elevated susceptibility of red colobus to infection following forest
fragmentation.
Comparisons of parasite prevalence can be a useful indirect indicator that parasites
may be impacting host populations (i.e., population declines correlated to increased
infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting red
colobus at higher prevalence in forest fragments have the capacity to cause substantial
pathology and death in primates (Table 3). High intensity infections of
Oesophogostomum sp. and Strongyloides sp. are associated with mucosal inflammation,
ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and

61
Johnsen 1978). Even moderate intensities of Oesophogostomum sp. have proven
clinically important in stressed captive primates (Crestian and Crespeau 1975; Soulsby
1982). For example, nearly 30% of 70 guenons imported to Italy from Senegal died soon
after arrival from severe oesophogostomiasis (Roperto et al 1985). Secondary bacterial
infections of mucosal lesions resulting in ulceration and fatal septicaemia are frequent
complications of oesophogostomiasis (Soulsby 1982). Thus, the elevated prevalence of
parasites infecting red colobus in forest fragments may contribute to greater morbidity
and mortality in this colobus population compared to the population inhabiting
undisturbed forests.
The magnitude and prevalence of multiple-species infections in individuals can be
another useful indirect indicator that parasites may be impacting host populations.
Multiple-species infections are associated with a greater potential for morbidity and
mortality due to synergistic and competitive interactions occurring between parasite
species (Nowak and May 1994; May and Nowak 1995; van Baalen and Sabelis 1995).
Consequently, the elevated frequency and number of multiple-species infections observed
in red colobus in forest fragments may contribute to greater morbidity and mortality in
this colobus population compared to the population inhabiting undisturbed forests.
My results demonstrate that humans, and potentially livestock, are exposing
colobus in forest fragments to novel pathogens. Four species infecting red colobus
(Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified strongyle)
and two species infecting black-and-white colobus (Ascaris sp. and an unidentified
strongyle) are likely anthropozoonotic or epizootic in origin. These parasites occur at
high frequency in the human populations in the region (NEMA 1997), but are absent

62
from colobus within Kibale National Park, where the people and primates interact at a
reduced frequency. In addition, the majority of colobine parasites appear to be
generalists and occur in the local human population (NEMA 1997). These are the
pathogens of greatest concern for rare species, such as the red colobus (Lafferty and
Gerber 2002). Humans and livestock may act as reservoirs, maintaining a high infection
risk for parasites that are detrimental to red colobus, even as red colobus densities decline
toward extinction (McCallum and Dobson 2002). Likewise, considering the extensive
overlap in parasite communities between the colobine species, black-and-white colobus
may also be acting as reservoirs for most red colobus parasites. Consequently, it will be
important to recognize the importance of generalist parasites within a community context
to preserve sensitive species, such as the endangered red colobus.
Our understanding of how anthropogenic habitat change alters wildlife disease
dynamics is in its infancy. Our comprehension of this interplay will be greatly improved
by future research that investigates how forest fragmentation and other forms of
anthropogenic habitat disturbance affect the rates and patterns of parasite transmission
within and among species. In addition, studies are needed that explore if and how
nutritional state modulates the effects of parasites and the occurrence of disease in wild
populations. Identifying risk factors for disease transmission will improve the ability of
conservationists to make rational decisions about the risks and benefits of extraction and
management activities.

Table 5-1. Prevalence (%) of gastrointestinal parasite infections in red colobus {Piliocolobus tephroceles) from forest fragments and
undisturbed forests in Kibale National Park, Uganda
Parasite Species
Fragmented (n = 390)
Undisturbed (n = 561)
Significance
Trichuris sp.
50
36
***
Unidentified strongyle
6
0
N.A.
Strongyloides fulleborni
5
4
N.S.
Strongyloides stercoralis
2
0
N.A.
Oesophagostomum sp.
4
2
*
As caris sp.
< 1
0
N.A.
Colobenterobius sp.
< 1
1
N.S.
Bertiella sp.
< 1
0
N.A.
Entamoeba coli
13
3
***
Entamoeba histolytica
10
3
**
Giardia lamblia
6
0
N.A.
Overall
50
37
***
* p < 0.05, ** p < 0.005, *** p < 0.001, N.S. p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence.

Table 5-2. Prevalence (%) of gastrointestinal parasite infections in black-and-white colobus (Colobus guereza) from forest fragments
and undisturbed forests in Kibale National Park, Uganda
Parasite Species
Fragmented (n = 94)
Undisturbed (n = 106)
Significance
Trichuris sp.
90
84
N.S.
Unidentified strongyle
5
0
N.A.
Strongyloides fulleborni
7
3
N.S.
Oesophagostomum sp.
4
9
N.S.
Asear is sp.
6
0
N.A.
Entamoeba coli
6
9
N.S.
Entamoeba histolytica
5
9
N.S.
Overall
90
84
N.S.
N.S.p > 0.05, N.A. no chi-square test performed since one forest type had 0 prevalence

Forest Fragmentation
Reduced Tree Density G Diversity
Reduced Habitat Area
Reduced Food Availability
Increased Contact with
Humans G Livestock
Restricted Ranging
y
Crowding Chronic Stress
Introduction of Novel Pathogens
y
Population Declines
Figure 5-1. Conceptual model of proposed mechanism for population declines in forest

5
en
>
O
en
O
C-
O
es
4
3
2
*
i
o
HMHH
(n = 561)
(n = 388)
Red Colobus
Undisturbed
Fragmented
T
(n = 100)
Black-and-White Colobus
as
as
Figure 5-2 Mean number of parasite species infecting individual red colobus (Pilocolobus tephrosceles), and black-and-white colobus
{Colobus guereza) in undisturbed and fragmented forest Western Uganda.

CHAPTER 6
VARIATION IN PRIMATE INFECTION DYNAMICS RELATES TO FOREST
FRAGMENT ATTRIBUTES
Introduction
For fragmented forests to have conservation value, they must retain ecological
integrity sufficiently to maintain species and biological processes over the long-term.
Studies have highlighted the importance of physical attributes such as fragment size,
shape, and isolation (Laurance and Bierregaard 1997); and biological attributes such as
predator, prey, and tree density and diversity on ecological processes and species survival
probabilities (Crooks and Soule 1999; Terborgh et al. 2001; Laurance et al. 2002).
However, despite the large scope of this research, our capacity to predict how ecological
processes will be altered and which taxonomic or functional groups will be most affected
by fragmentation is still poor.
Such difficulties are well illustrated by primates inhabiting forest fragments. No
clear generalizations emerge as to what types of primates are most susceptible to
fragmentation, nor what types of fragments are most likely to support primates, despite a
growing body of research (Tutin et al. 1997; Onderdonk and Chapman 2000; Marsh
2003). Our inability to evaluate the potential of forest fragments for primate conservation
appears to be driven by several factors. First, most previous work has been conducted in
fragments protected from human use (Lovejoy et al. 1996; Tutin et al. 1997; Gilbert
2003); however, typically fragments are not protected and are characterized by open
access by private citizens who depend on them for fuelwood, medicinis, or bushmeat
67

68
(Chapman et al. 2003). While studies involving protected fragments have provided us
with many insights, they may have biased our perception of the value of forest fragments
for conservation.
Second, a number of simple logical predictions relating to primates in forest
fragments have not proven to be general. For example, home range size was frequently
cited as influencing a species ability to survive in a fragment (Lovejoy et al 1986; Estrada
and Coates-Estrada 1996). However, Onderdonk and Chapman (2000) found no
relationship between home range size and ability to live in fragments for a community of
primates in western Uganda. Similarly, it has been suggested that a highly frugivorous
diet may limit the ability of a species to live in fragments (Lovejoy et al 1986; Estrada
and Coates-Estrada 1996). However, Tutin et al. (1997) found that several frugivorous
species were at higher or similar densities in forest fragments than in the intact forest of
Lop Reserve, Gabon (see also Tutin 1999; Onderdonk and Chapman 2000).
Lastly, past studies have often focused on simple correlates to primate population
viability in forest fragments. However, finding such single correlative explanations for
complex biological phenomena, like determinants of primate abundance in fragments, is
unlikely. Rather, recent long-term studies have highlighted the importance of
multifactoral explanations. For example, based on a 68-month study of howler monkeys
(Alouatta palliata) and a parasitic bot fly (Alouattamyia baeri), Milton (1996) concluded
that the annual pattern of howler mortality results from a combination of effects
including: age, physical condition, and larval burden of the parasitized individual, which
becomes critical when the population experiences dietary stress (see also Milton et al.
1994). Similarly, Gulland (1992) studied the interactions of Soay sheep and nematode

69
parasites and demonstrated that at times of population crashes sheep were emaciated, had
high nematode burdens, and showed signs of protein-energy malnutrition. In the field,
sheep treated with antihelminthics had lower mortality rates, while experimentally
infected sheep with high parasite loads, but fed nutritious diets, showed no sign of
malnutrition. The potential role of parasites and infectious disease in primate population
dynamics in forest fragments remains largely unexplored.
Helminthic and protozoal parasites can impact host survival and reproduction
directly through pathological effects and indirectly by reducing host condition (Chandra
and Newbeme 1977; Boyce 1990; Dobson and Hudson 1992; Hudson et al. 1992; Coop
and Holmes 1996). Severe parasitosis can lead to blood loss, tissue damage, spontaneous
abortion, congenital malformations, and death (Chandra and Newbeme 1977;
Despommier et al. 1995). However, less severe infections are more common and may
impair nutrition, travel, feeding, predator escape, and competition for resources or mates;
or increase energy expenditure (Dobson and Hudson 1992; Hudson et al. 1992; Coop and
Holmes 1996; Stien et al. 2002; Packer et al. 2003). Through these proximate
mechanisms, parasites can potentially regulate host populations (Gregory and Hudson
2000; Hochachka and Dhondt 2000).
To improve our capacity to evaluate the conservation value of forest fragments, I
examined how various fragment attributes affect one ecological process, parasite
infection dynamics, and consider how changes in this process may impact host
populations of red colobus (Piliocolobus tephrosceles) inhabiting a series of forest
fragments in western Uganda.

70
Materials and Methods
Study Site
Nine forest fragments that support red colobus that lie within the agricultural
landscape adjacent to the western boundary of Kibale National Park and in the foothills
of the Ruwenzori Mountains in Uganda were surveyed. Mean annual rainfall in the
region is 1749 mm (1990-2001) and mean daily minimum and maximum temperatures
are 14.9C and 20.2C (1990-2001). Rainfall is bimodal, with two rainy seasons
generally occurring from March to May and September to November.
Prior to agricultural expansion; mid-elevation, moist, evergreen forest dominated
the region (Naughton-Treves 1997). While the precise timing of isolation of these forest
remnants is not known, local elders describe them as 'ancestral forests', and aerial
photographs from 1959 confirm that most have been isolated from Kibale since at least
that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha and occur in
areas largely unsuitable for agriculture (i.e., forested swampy valley bottoms, steep
forested rims of crater lakes; Table 6-1). These fragments are used by local citizens to
varying degrees and are surrounded by small-scale agriculture or tea plantations (Table 6-
1).
Fecal Sampling and Analysis
From August 1999 to July 2003,1 collected 536 fecal samples from red colobus in
forest fragments to determine the prevalence of infection with strongyle and rhabditoid
nematodes, a group of potentially pathogenic parasites. All samples were collected
immediately after defecation to avoid contamination and examined macroscopically for
adult nematodes. Samples were stored individually in 5.0 mL sterile vials in a 10%
neutral formalin solution. Preserved samples were transported to the University of

71
Florida where they were examined for nematode eggs and larvae using concentration by
sodium nitrate flotation and fecal sedimentation (Sloss et al. 1994). Nematodes were
counted and identified on the basis of egg color, shape, contents, and size. Measurements
were made to the nearest 0.1 micron SD using an ocular micrometer fitted to a
compound microscope. Coprocultures and necropsies (MAFF 1979) were used to match
nematode eggs to larvae and adult worms for positive identification.
Infection Risk Assessment
To obtain an index of infection risk, I determined infective-stage parasite densities
for canopy vegetation, ground vegetation, and soil plots from fragments with high stump
density (Kiko 3) and low stump density (Nkuruba). From January to August 2002,1
collected thirty 1 m3 vegetation plots at a height of 12 m from canopy trees used within
the previous two hours by red colobus; 15 from each fragment. Canopy access for plot
collection was facilitated by single rope climbing technique (Mitchell, 1982; Laman,
1995, Houle et al. 2004). Thirty 1 m3 ground vegetation plots were collected below all
trees sampled for canopy plots. Soil plots (0.05 m3 surface scratches) were collected
within randomly selected ground vegetation plots, 10 from forest fragments and 10 from
undisturbed forest. I used a modified sedimentation technique to recover infective-stage
parasites from vegetative plots (Sloss et al. 1994). Soil plots were examined using a
modified Baermann method (Sloss et al. 1994). Samples were examined by dissecting
and compound scope, and infective-stage individuals of the most prevalent strongyle
nematode, Oespohagostomum sp. (L3 larvae) were counted.
Fragment Characteristics
Forest fragment attributes quantified included fragment size, fragment type,
distance to Kibale, distance to the nearest fragment, trees/ha, tree species/ha, tree

72
stumps/ha, red colobus/ha, and total colobines/ha. The size of each fragment was
measured, taking GPS readings at locations along fragment edges and/or measuring
fragment perimeters with a 50 m tape (Onderdonk and Chapman 2000). Fragments were
classified as crater lake, hillside, or valley bottom. Crater lake and hillside fragments (n
= 4) were forests on steep hills or sides of explosion craters; for analyses, they are
considered together. Valley-bottom fragments (n = 5) have swamp vegetation associated
with their lowest levels. Consequently, valley-bottom fragments may retain greater
humidity, potentially providing a better environment for the development of strongyle
nematodes during their free-living stage. Distance to Kibale National Park and nearest
fragment are straight-line distances measured from topographic maps. At each fragment,
all trees > 10 cm DBH (Diameter at Breast Height; Chapman et al. 2003) were identified
and measured. Sizes of trees on very steep craters were visually estimated (error in visual
estimation = + 3.7%, N = 46). As colobus rarely feed in small trees (Gillespie and
Chapman 2001), this represents a nearly complete inventory of all colobus potential food
sources. Tree stumps remaining after harvest by local people were also counted. This
involved carefully searching through vine tangles and dense herbaceous vegetation in
search of hidden stumps. For most tree species, the stump will remain for several years,
providing an index of habitat degradation.
Since parasite dynamics could be influenced by host density, the density of red
colobus and black-and-white colobus (Colobus guereza) were determined via
observations made over 24-hours at each fragment. I include red colobus, as well as total
colobus, density among biological attributes examined, since black-and-white colobus
may serve as a reservoir host for red colobus infection with shared parasites.

73
Results
Mean fragment size for the 9 fragments surveyed was 5.11 ha and fragments ranged
from 1.20 to 8.70 ha (Table 6-1). Five of the fragments were classified as valley bottom
and 4 were crater lake or hillside (Table 6-1). Mean distance to Kibale National Park was
2.4 km and ranged from 0.2 to 6.5 km (Table 6-1). Mean distance to the nearest fragment
was 142 m and ranged from 50 (the criteria for a isolated fragment) to 500 m (Table 6-1).
Mean tree density was 133 trees/ha and ranged from 27 to 445 trees/ha (Table 6-1).
Mean tree species/ha was 15.9 tree species/ha and ranged from 4 to 73 tree species/ha
(Table 6-1). The level of degradation of the fragments was highly variable and stump
density ranged from 0.16 to 221.76 stumps/ha and averaged 69.2 stumps/ha (Table 6-1).
Stumps density reflects the intensity of extraction in these fragments, which was
associated with beer brewing, gin distillation, and charcoal production by households
bordering a fragment (Chapman et al 2003). Red colobus density averaged 3.70 red
colobus/ha and ranged from 0.55 to 8.33 red colobus/ha (Table 6-1). Mean colobine
density (red colobus and black-and-white colobus) was 5.52 colobines/ha and ranged
from 1.66 to 9.41 colobines/ha (Table 6-1).
Two strongyle (Oespohagostomum sp. and an unidentified strongyle) and 2
rhabditoid nematodes (Strongyloides fulleborni and S. stercoralis) were found from red
colobus inhabiting forest fragments (Table 6-2). Mean prevalence among fragments of
Oespohagostomum sp. was 5%, but prevalence ranged from 0 to 24 %. Mean prevalence
of the unidentified strongyle was 8% and ranged from 0 to 28%. S. fulleborni prevalence
averaged 6% among fragments and ranged from 0 to 16%. The prevalence of S.
stercoralis was the lowest of all nematodes examined averaging 2% among fragments,

74
but it ranged from 0 to 12. Collectively, the prevalence of strongyles and rhabditoids was
20% and ranged from < 1% to 68%.
Individually and collectively, the prevalence of all strongyle and rhabditoid
nematodes was positively correlated with stump density (Table 6-3). With the exception
of Oespohagostomum sp., prevalence of all strongyles and rhabditoids individually and
collectively, was negatively correlated with fragment size (Table 6-3). Strongyloides
stercoralis prevalence was positively correlated with red colobus and total colobine
density (Table 6-3).
When predicting strongyle and rhabditoid prevalence using a step-wise multiple
regression that included stump density, fragment size, and colobus density; stump density
entered the model first explaining 85% of the variance (F = 38.84, R = 0.847, P < 0.001).
Subsequently, no other variable entered the model suggesting that fragment degradation,
indexed by stump density, was the most important variable in predicting strongyle and
rhabditoid prevalence and once this variable was considered, there was little remaining
variance that could be explained by other variables measured. Stump density was
correlated with fragment size (r=-0.811, P= 0.008), and colobus density (r=0.657,
P-0.054).
A similar situation was found when predicting Oespohagostomum sp. (F = 13.41,
R2 = 0.608, P = 0.008), S. fulleborni (F = 21.64, R2 = 0.756, P = 0.002), S. stercoralis (F
= 71.66, R2 = 0.911, P < 0.001), and the unidentified strongyle prevalence (F = 9.93, R2 =
0.587, P = 0.016), in that only stump density entered the model.
Oesophagostomum sp. L3 larvae were more abundant in ground vegetation plots
from Kiko 3, the fragment with high stump density, compared to Nkuruba, which had

75
low stump density (Kiko 3 mean = 3.33 0.64 larvae/m3, Nkuruba mean = 0.82 0.98
larvae/m3, t= -2.87, P = 0.005). However, Oesophagostomum sp. L3 larvae were not
found in canopy or soil plots.
Discussion
The results of this study demonstrate that an index of habitat degradation, stump
density, best explained the prevalence of strongyle and rhabditoid nematode infections in
red colobus in forest fragments in western Uganda. I also found a greater risk of
infection with Oesophagostomum sp., a representative strongyle, for red colobus in the
fragment with the highest stump density compared to the fragment with the lowest stump
density. In some cases, fragment size and colobine density were also related to strongyle
and rhabditoid prevalence, but these variables did not explain a significant amount of
variation that was independent of stump density.
These results may provide insights into observed declines in red colobus in the
forest fragments of western Uganda. As noted earlier, red colobus declined in these
forest fragments by 20% between surveys in 2000 and 2003. Altered parasite dynamics
may play a role in these declines. Although parasite infections are common in nature and
low-intensity infections are often asymptomatic (Anderson and May 1979; May and
Anderson 1979), anthropogenic change may result in altered transmission rates, parasite
host range, and parasite virulence (Daszak et al. 2000; Patz et al. 2000). Resultant
changes in host susceptibility may result in elevated morbidity and mortality, and
ultimately, population declines.
The strongyle and rhabditoid nematodes documented to infect red colobus in this
study have the capacity to cause substantial pathology and death in primates. Heavy
infections of Oesophogostomum spp. and Strongyloides spp. have been associated with

76
mucosal inflammation, ulceration, dysentery, weight loss, and death in primates
(McClure and Guilloud 1971; DePaoli and Johnsen 1978; Holmes et al. 1980; Harper et
al. 1982). Even moderate intensities of Oesophagostomum sp. have proven important in
stressed or captive primates (Crestian and Crespaeu 1975; Soulsby 1982). For example,
nearly 30% of 70 guenons imported to Italy from Senegal died soon after arrival from
severe oesophogostomiasis (Roperto et al. 1985). Secondary bacterial infections of
mucosal lesions resulting in ulceration and fatal septicaemia are frequent complications
of oesophogostomiasis (Soulsby 1982). Even more troubling are S. stercoralis and
unidentified strongyle infections, which are likely anthropozoonotic in origin. These
parasites occur at high frequency in the human populations in the region, but are absent
from colobus within Kibale National Park, where the people and primates interact at a
reduced frequency. Since S. stercoralis parasitic females live in the superficial tissues of
the small intestine, and can be present in high numbers due to autoinfection, they can
cause significant pathology in humans (Pappas and Wardrop 1999).
Considering the potential role that strongyle and rhabditoid nematode infections
may play in red colobus declines in forest fragments, we should investigate ways to
mitigate alterations in infection dynamics in the face of extraction.

Table 6-1. Physical and biological attributes of forest fragments with red colobus (Piliocolobus tephroceles) populations near Kibale
National Park, Uganda
Fragment
Size (ha)
Fragment
Type
Distance to
Kibale (km)
Nearest
Fragment (m)
Trees/ha
Tree species/ha
Stumps/ha
Red Colobus/ha
Colobines/ha
Bugembe
4.68
VB
2.5
500
52
8.76
71.18
2.35
2.35
CK
8.70
HS
0.2
150
41
4.94
45.75
2.87
3.68
Kifuruka
7.24
CL
6.5
95
27
4.03
12.42
0.55
1.66
Kiko 1
6.20
VB
2.0
50
42
6.61
56.45
3.55
4.19
Kiko 2
5.00
VB
1.8
125
63
4.00
8.40
2.80
5.20
Kiko 3
1.70
VB
1.1
70
231
12.94
221.76
4.71
9.41
Kiko 4
1.20
VB
1.1
70
259
20.83
174.17
8.33
8.33
Nkuruba
6.40
CL
3.6
70
445
73.00
0.16
3.44
6.72
Rutoma
4.90
HS
3.0
150
34
7.76
32.24
4.69
8.16
Average
5.11
N.A.
2.4
142
133
15.87
69.17
3.70
5.52

Table 6-2. Prevalence (%) of strongyle and rhabditoid nematode infections in red colobus monkeys (Piliocolobus tephroceles) in
forest fragments near Kibale National Park, Uganda
Fragment
N
Oesophagostomum sp.
Unidentified Strongyle
Strongyloides fulleborni
Strongyloides stercoralis
Collective
Bugembe
31
3
16
6
0
25
CK
66
2
2
0
0
4
Kifuruka
53
2
0
4
0
6
Kiko 1
45
5
9
11
9
34
Kiko 2
40
7
0
9
0
16
Kiko 3
25
24
28
16
12
68
Kiko 4
44
3
9
5
0
17
Nkuruba
179
< 1
0
0
0
< 1
Rutoma
53
0
6
0
0
6
Average
N.A.
5
8
6
2
20

Table 6-3.Correlation matrix of stongyle and rhabditoid nematode prevalence in red colobus monkeys (Piliocolobus tephrosceles) and
attributes of the forest fragments they inhabit near Kibale National Park, Uganda
Oesophagostomum sp. Unidentified Strongyle Strongyloides fullebomi Strongyloides stercoralis Collective
Fragment Size
-0.581 (p = 0.101)
-0.730 (p = 0.025) *
-0.777 (p = 0.014)**
-0.835 (p = 0.005) **
-0.811 (p = 0.008)
Fragment Type
-0.220 (p = 0.570)
-0.409 (p = 0.274)
0.049 (p = 0.901)
-0.014 (p = 0.971)
-0.185 (p = 0.634)
Distance to Kibale
-0.336 (p = 0.377)
-0.393 (p = 0.296)
-0.328 (p = 0.389)
-0.401 (p = 0.285)
-0.417 (p = 0.264)
Nearest Fragment
-0.204 (p = 0.598)
0.285 (p = 0.458)
-0.121 (p = 0.757)
-0.291 (p = 0.448)
-0.019 (p = 0.962)
Trees / ha
0.201 (p = 0.605)
0.109 (p = 0.780)
0.142 (p = 0.715)
0.422 (p = 0.258)
0.199 (p = 0.608)
Tree sp. / ha
-0.128 (p = 0.744)
-0.199 (p = 0.607)
-0.226 (p = 0.560)
0.012 (p = 0.976)
-0.184 (p = 0.635)
Red Colobus / ha
0.239 (p = 0.536)
0.010 (p = 0.980)
0.442 (p = 0.234)
0.672 (p = 0.047) *
0.437 (p = 0.240)
Colobines / ha
0.459 (p = 0.214)
0.267 (p = 0.487)
0.367 (p = 0.331)
0.691 (p = 0.039) *
0.511 (p = 0.160)
Stumps / ha
0.811 (p = 0.008) **
0.766 (p = 0.016)**
0.869 (p = 0.002) **
0.954 (p< 0.001)**
0.920 (p< 0.001)
(n 9 for all comparisons, Pearson Correlation and corresponding P-value provided)

CHAPTER 7
SUMMARY AND CONCLUSIONS
Emerging infectious diseases have raised global awareness of the potential impact
that ecological change can have on biodiversity conservation and wildlife and human
health. This study improves our understanding of this interplay by examining the effects
of logging and forest fragmentation on parasite dynamics in an African primate
community. The most important contributions of this study are as follows.
1. This study provided the first reports of gastrointestinal helminth parasites from wild
populations of redtail guenons, l'hoesti monkeys, red colobus, and black-and-white
colobus and the first report of gastrointestinal helminth parasites from blue and
vervet monkeys from Uganda. This baseline data on the patterns of parasitic
infection in wild monkeys provides a first step toward an index of population health
and disease risk assessment for conservation and management plans of threatened
and endangered African primate populations.
2. This study demonstrated that selective logging was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus, black-and-white colobus, and redtail guenons. Despite
this higher infection risk for all species, only redtail guenons manifested higher
prevalence and richness of gastrointestinal parasite infections and greater
magnitude multiple-infections in logged compared to undisturbed forests. These
results suggest that redtail guenons are more susceptible to parasitic infection
following selective logging than colobines.
3. This study demonstrated that forest fragmentation was associated with altered
infection dynamics resulting in higher densities of infective-stage parasites
common to red colobus and black-and-white colobus. Despite this higher infection
risk for both species, only red colobus manifested higher prevalence and richness of
gastrointestinal parasite infections and greater magnitude muliple-infections in
fragmented compared to undisturbed forests. These results suggest that red colobus
are more susceptible to parasitic infection following forest fragmentation than
black-and-white colobus.
4. This study demonstrated that humans, and potentially livestock, are exposing
colobus in forest fragments to novel pathogens. Four species infecting red colobus
(Strongyloides stercoralis, Ascaris sp., Giardia lamblia, and an unidentified
80

81
strongyle) and two species infecting black-and-white colobus (Ascaris sp. and an
unidentified strongyle) are likely anthropozoonotic or epizootic in origin. These
parasites occur at high frequency in the human populations in the region, but are
absent from colobus within Kibale National Park, where the people and primates
interact at a reduced frequency.
5. This study demonstrated that an index of habitat degradation, stump density, best
explained the prevalence of strongyle and rhabditoid nematode infections in red
colobus in forest fragments in western Uganda. This coincided with a greater risk
of infection with Oesophagostomum sp.,a representative strongyle nematode, for
red colobus in the fragment with the highest stump density compared to the
fragment with the lowest stump density. Considering the potential role that these
nematode infections may play in red colobus declines in forest fragments, future
studies should investigate ways to mitigate alterations in infection dynamics in the
face of extraction.

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Adedeji S.O., E.O. Ogunba, and O.O. Dipeolu. 1989. Synergistic effect of migrating
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BIOGRAPHICAL SKETCH
Thomas R. Gillespie was bom in Rockford, IL, on 16 September 1974. Gillespie
received his B.Sc. in Ecology, Ethology, and Evolution in May 1996 from the University
of Illinois, Urbana-Champaign. After completing his undergraduate studies, he worked
with the Universidad Nacional de la Amazonia Peruana and Dr. Carl Bouton of the
University of Illinois to develop and establish a semi-autonomous environmental
education program for the school system of Iquitos, Peru. He joined the department of
zoology at the University of Florida in 1997 and, working with Dr. Colin A. Chapman,
was awarded his M.Sc. in 2000. For the past seven years, he has been working with
African, European, and North American colleagues on a long-term investigation of the
effects of anthropogenic disturbance (i.e., selective logging and forest fragmentation) on
the ecology and behavior of wildlife in Kibale National Park and surrounding areas in
Uganda. Since 1999, parasite and disease dynamics have become central to his role in
these collaborations. Gillespie is a STAR fellow of the United States Environmental
Protection Agency, a member of the IUCN Veterinary Specialist Groups Great Ape
Health Monitoring Unit (GAHMU), serves on a national advisory committee to Amnesty
International on topics at the nexus of conservation and human rights, and assists the
BBC Natural History Unit as a biological consultant.
99

I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
l a-
Colin A. Chapman, Chair 7
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Sue Boinski
Associate Professor of Anthropology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
? 2C
J. Chapman
Professor of Zoology
I certify that have read this study and that in my opinion it conf
standards of scholarly presentation and is fully adequate,jn
dissertation for the degree of Doctor of Philosopf
s to acceptable
ality, as a
Greine
Professor of Veterinary Medicine
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Michael A. Huffman
Associate Professor of Ecology, Kyoto
University, Japan

This dissertation was submitted to the Graduate Faculty of the Department of
Zoology in the College of Liberal Arts and Sciences and to the Graduate School and was
accepted as partial fulfillment of the requirements for the degree of Doctor of Philosophy.
August 2004
Dean, Graduate School



4
to unlogged forest. Moreover, group densities of Cercopithecus ascanius and C. mitis in
high-intensity logged forest continued to decline even 28 years after logging (Chapman et
al. 2000). In contrast, the density of eastern black-and-white colobus (Colobus guereza)
was not lower in logged compared to undisturbed forest at both 12 and 28 years after
logging (Skorupa 1988, Chapman et al. 2000). Thus, although some primate species may
cope well with high-intensity selective logging, the majority of primates fair poorly.
Although forest fragmentation and high-intensity, selective logging are known to
negatively impact primate abundance and species richness, little is known about the
proximate mechanisms responsible for such effects. To successfully combat species loss
in such systems, we must understand the underlying mechanisms of species loss. Parasite
dynamics may be one such mechanism.
Animal populations are largely regulated by three factors: availability of quality
food, predation, and infectious disease (Lack 1954; Minchella and Scott 1991; Dobson
1995). While a great deal of research has focused on the effects of food availability and
predation on primate abundance (Struhsaker 1976; Milton 1982; Isbell 1990; Struhsaker
and Leaky 1990; Chapman and Chapman 1999), the role of infectious disease has
remained largely unexplored (Stuart and Strier 1995). Forest fragmentation and high-
intensity, selective logging may alter primate-parasite dynamics (resulting in higher rates
of primate mortality, lower reproductive rates, and debilitation). Consequently, an
understanding of how these manifestations of human disturbance affect primate-parasite
dynamics could be of central importance in designing effective conservation and
management plans.


ACKNOWLEDGMENTS
I thank my advisor, Colin Chapman, whose support and assistance were invaluable
during this work. His expertise and enthusiasm provided a solid foundation for this study.
I owe much to my committee members (Drs. Sue Boinski, Lauren Chapman, Ellis
Greiner, and Michael Huffman) for their advice and support throughout this venture.
Drs. Andy Dobson, Donald Forrester, Robert Holt, William Karesh, Joanna Lambert,
Arthur Mugisha, Thomas Struhsaker, and the honorable Betty Udongo shared insights
that improved this work.
I am grateful to Dennis Sebugwawo and all employees of the Kibale Fish and
Monkey Project for their hard work and dedication. I am grateful to Stacey Bonovitch,
Lauren Castleberry, Brian Davidson, John Davis, Jennifer Davis-Summer, Erin Ehmke,
Kristen Guttmann, Sarah Hawkins, Joe Mahoney, Anjan Patel, Michelle Roman, May
Stewart, Gregory Zhelesnik, and Jennifer Zipser for their assistance in the laboratory. I
thank my many colleagues at Kibale National Park, Uganda, and the University of
Florida who have shared insight, advice, friendship, and humor. Especially Evelina
Jagminaite who saw me through much of this work.
I am ever grateful to my parents, Robert and Margaret Gillespie, who have been a
constant source of encouragement and support throughout my life.
This research has been supported by grants from the National Center for
Environmental Research of the United States Environmental Protection Agency (STAR
Fellowship), the National Science Foundation (grant number SBR-990899), the Wildlife
iii


60
This appears to be the case for the red colobus. Red colobus typically consume a high
diversity diet (i.e., > 42 species) and their density can be predicted from the abundance of
important food trees (Struhsaker 1975; Chapman et al. 2002). Such broad dietary
requirements might predispose red colobus to food stress in forest fragments, where the
necessary diversity of plant species and parts are not always available (Chapman et al.
2003b). In contrast, black-and-white colobus have a low diversity diet (i.e., < 25 species
with 3 species accounting for 69%) and demonstrate a high degree of dietary flexibility
(Onderdonk and Chapman 2000; Oates 1974). They are clearly capable of persisting on a
monotonous diet dominated by readily available tree species, an advantage for living in
forest fragments with high variation in tree species composition (Chapman et al. 2003b).
However, one population of red colobus has been documented to persist on a very
monotonous diet (Chapman et al. 2002) and as fragments are degraded red colobus are
often the last species to remain. Correlating stress hormones with variation in food
availability and quality would provide insights into whether or not this factor is
responsible for this elevated susceptibility of red colobus to infection following forest
fragmentation.
Comparisons of parasite prevalence can be a useful indirect indicator that parasites
may be impacting host populations (i.e., population declines correlated to increased
infection prevalence; McCallum and Dobson 1995). Several of the parasites infecting red
colobus at higher prevalence in forest fragments have the capacity to cause substantial
pathology and death in primates (Table 3). High intensity infections of
Oesophogostomum sp. and Strongyloides sp. are associated with mucosal inflammation,
ulceration, dysentery, weight loss, and death (McClure and Guilloud 1971; DePaoli and


70
Materials and Methods
Study Site
Nine forest fragments that support red colobus that lie within the agricultural
landscape adjacent to the western boundary of Kibale National Park and in the foothills
of the Ruwenzori Mountains in Uganda were surveyed. Mean annual rainfall in the
region is 1749 mm (1990-2001) and mean daily minimum and maximum temperatures
are 14.9C and 20.2C (1990-2001). Rainfall is bimodal, with two rainy seasons
generally occurring from March to May and September to November.
Prior to agricultural expansion; mid-elevation, moist, evergreen forest dominated
the region (Naughton-Treves 1997). While the precise timing of isolation of these forest
remnants is not known, local elders describe them as 'ancestral forests', and aerial
photographs from 1959 confirm that most have been isolated from Kibale since at least
that time (Chapman et al. 2003). Fragments range in size from 1.2 to 8.7 ha and occur in
areas largely unsuitable for agriculture (i.e., forested swampy valley bottoms, steep
forested rims of crater lakes; Table 6-1). These fragments are used by local citizens to
varying degrees and are surrounded by small-scale agriculture or tea plantations (Table 6-
1).
Fecal Sampling and Analysis
From August 1999 to July 2003,1 collected 536 fecal samples from red colobus in
forest fragments to determine the prevalence of infection with strongyle and rhabditoid
nematodes, a group of potentially pathogenic parasites. All samples were collected
immediately after defecation to avoid contamination and examined macroscopically for
adult nematodes. Samples were stored individually in 5.0 mL sterile vials in a 10%
neutral formalin solution. Preserved samples were transported to the University of


9
of the study are presented in Chapter 4. I made a similar comparison, examining
infection dynamics for red colobus and black-and-white colobus between forest
fragments and undisturbed forest. Details of this aspect of the study are presented in
Chapter 5. Finally, I examined the relationship among physical and biological attributes
of forest fragments and strongyle nematode infection dynamics in red colobus. Details of
this aspect of the study are presented in Chapter 6.


I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
l a-
Colin A. Chapman, Chair 7
Professor of Zoology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Sue Boinski
Associate Professor of Anthropology
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
? 2C
J. Chapman
Professor of Zoology
I certify that have read this study and that in my opinion it conf
standards of scholarly presentation and is fully adequate,jn
dissertation for the degree of Doctor of Philosopf
s to acceptable
ality, as a
Greine
Professor of Veterinary Medicine
I certify that I have read this study and that in my opinion it conforms to acceptable
standards of scholarly presentation and is fully adequate, in scope and quality, as a
dissertation for the degree of Doctor of Philosophy.
Michael A. Huffman
Associate Professor of Ecology, Kyoto
University, Japan