Human Behavior and Opportunities for Parasite Transmission in Communities Surrounding Long Tailed Macaque Populations in Bali, Indonesia.

American Journal of Primatology 76:159–167 (2014)

RESEARCH ARTICLE
Human Behavior and Opportunities for Parasite Transmission in Communities
Surrounding Long‐Tailed Macaque Populations in Bali, Indonesia
KELLY E. LANE‐DeGRAAF1*, I.G.A. ARTA PUTRA2, I. NENGAH WANDIA2, AIDA ROMPIS2, HOPE HOLLOCHER1,
3
AND AGUSTIN FUENTES
1
Department of Biological Sciences, University of Notre Dame, Notre Dame,
2
Primate Research Center, Udayana University, Denpasar, Bali, Indonesia
3

Indiana

Department of Anthropology, University of Notre Dame, Notre Dame, Indiana

Spatial overlap and shared resources between humans and wildlife can exacerbate parasite
transmission dynamics. In Bali, Indonesia, an agricultural‐religious temple system provides
sanctuaries for long‐tailed macaques (Macaca fascicularis), concentrating them in areas in close

proximity to humans. In this study, we interviewed individuals in communities surrounding 13 macaque
populations about their willingness to participate in behaviors that would put them at risk of exposure to
gastrointestinal parasites to understand if age, education level, or occupation are significant
determinants of exposure behaviors. These exposure risk behaviors and attitudes include fear of
macaques, direct contact with macaques, owning pet macaques, hunting and eating macaques, and
overlapping water uses. We find that willingness to participate in exposure risk behaviors are correlated
with an individual’s occupation, age, and/or education level. We also found that because the actual risk of
infection varies across populations, activities such as direct macaque contact and pet ownership, could be
putting individuals at real risk in certain contexts. Thus, we show that human demographics and social
structure can influence willingness to participate in behaviors putting them at increased risk for
exposure to parasites. Am. J. Primatol. 76:159–167, 2014. © 2013 Wiley Periodicals, Inc.
Key words:

risk; gut parasite; long‐tailed macaques; human behavior

INTRODUCTION
Transmission of zoonotic parasites often occurs
when high‐density human and wildlife populations
coexist and share resources [Daszak and Cunnigham,
2003; Daszak et al., 2001; Jones‐Engel et al., 2008;

Murphy, 1998; Wolfe et al., 1998]. While land use
practices that affect human–wildlife interactions are
recognized as important in widespread parasite
transmission, the mechanisms of parasite transmission events in the landscape are not fully understood.
In particular, how human–wildlife interactions and
land use practices enhance transmission opportunities, especially for gastrointestinal parasites, is
largely neglected [Lafferty and Gerber, 2002; Nunn
and Altizer, 2006]. The source of many diarrheal
infections, one of the most common causes of
mortality and morbidity in the developing world
[Alum et al., 2010; Cleaveland et al., 2001; Stepek
et al., 2006; WHO, 2007], is exposure to infected feces
or contaminated water. Many gastrointestinal parasites are transmissible in water, enabling them to
spread beyond the source of the original infection
[Cleaveland et al., 2001; Meyer, 1985; WHO, 2007].
Gastrointestinal parasites, especially those transmitted through the fecal–oral route, can produce

© 2013 Wiley Periodicals, Inc.

environmentally viable infectious stages, increasing

the risk of exposure via contaminated soil or water
long after the infective stage was deposited. The
impact of diarrheal diseases is drastically greater in
regions of the world where access to clean water and
public sanitation measures may be limited [Alum
et al., 2010; Stepek et al., 2006; WHO, 2007].
On the island of Bali, Indonesia, increases in
human density have substantially increased the
frequency of contact between humans and long‐tailed

Contract grant sponsor: National Science Foundation;
contract grant number: BSC‐0639787; contract grant sponsor:
University of Notre Dame’s Institute for Scholarship in the
Liberal Arts
Conflicts of interest: None.


Correspondence to: Kelly E. Lane‐deGraaf, Odum School of
Ecology, University of Georgia, Athens, GA 30602.
E‐mail: lanedegraaf.kelly@gmail.com

Received 8 April 2013; revised 26 August 2013; revision
accepted 28 August 2013
DOI: 10.1002/ajp.22218
Published online 1 October 2013 in Wiley Online Library
(wileyonlinelibrary.com).

160 / Lane‐deGraaf et al.

macaques (Macaca fascicularis), especially in areas
where they coexist [Fuentes et al., 2005; Jones‐Engel
et al., 2008]. Non‐human primates, including long‐
tailed macaques, have been identified as hosts and
reservoirs of several infectious diseases found in
humans, including microfilariasis, giardiasis, enterobiasis, and schistosomiasis [Alum et al., 2010; Fuller
et al., 1979; Hahn et al., 2000; Huffman and
Chapman, 2009; Mak et al., 1982; Nunn and Altizer,
2006; Pederson et al., 2005; Taylor et al., 2001; Wolfe
et al., 2004], and recently, simian foamy virus (SVF)
was detected among humans living and working in
Balinese monkey forests [Jones‐Engel et al., 2004].

Given that many primates are a potential source of
parasite risk for humans, it is central to understand
how human behaviors may potentially facilitate
exposure to and transmission of these parasites.
The long‐tailed macaque is found throughout
Southeast Asia, including Bali, Indonesia, where a
system of agricultural‐religious temples exists
[Fuentes et al., 2005; Lansing, 1995; Lane, 2010].
Relatively large macaque populations live at monkey
forests, or community temple sites, surrounded by
remnant forest patches and often linked by streams
and rivers (Fig. 1). The maintenance of resident
populations of macaques at these temples demonstrates a dichotomy of attitude among the Balinese.
Macaques figure prominently in Balinese Hindu
philosophy and tradition, and it is this role in culture
that has led some to suggest a sacredness of
macaques [Wheatley, 1999]. However, evidence has
revealed that this view is highly context dependent

[Loudon et al., 2006; Schillaci et al., 2010], with

different treatment of macaques inside versus
outside of temple complexes. Recent reductions in
overall forest cover on the island have resulted in a
number of high‐density macaque populations co‐
occurring in areas of high‐density human communities, some with densities reaching as high as 500
people/km2 [Fuentes et al., 2005; Wheatley, 1999].
The Balinese landscape reflects the island’s economic
shift from traditional rice agriculture towards international tourism over the last four decades, resulting
in an increase in urban development and reduction in
land dedicated to rice agriculture [Fuentes et al.,
2005; Lane et al., 2010; Lansing, 2007]. This change
in land use has brought human and macaque
populations closer together, living around temple
sites and sharing community water sources, and
potentially increasing the risk of non‐human primate‐to‐human parasite exposure.
The ability of human attitudes to directly
influence their behaviors has been demonstrated
repeatedly [Eyal and Kunkel 2008; Stulhofer et al.,
2007]. McCleery [2009], studying urban wildlife–
human aggression, demonstrated that attitudes

towards wildlife can be changed, and that predictive
models of wildlife–human interactions are more
accurate when human attitudes and beliefs are
included in these models. This point is especially
salient given recent work demonstrating macaque‐to‐
human transmission of SFV and human‐to‐macaque
transmission of gastrointestinal parasites with pet
macaques [Jones‐Engel et al., 2004, 2005, 2008] and

Fig. 1. Map of Bali with monkey forest distribution. Populations marked in black represent those temple sites in which surveys were
performed.

Am. J. Primatol.

Behavior and Parasite Exposure Risk / 161

could be important in identifying opportunities to
reduce parasite transmission opportunities wherever
human and non‐human primate populations coexist
[Altizer and Nunn, 2006; Gillespie et al., 2005;

Goldberg et al., 2008; Wolfe et al., 1998, 2004,
2007]. Differences in attitude towards long‐tailed
macaques, related to occupation, education level, and
age could prove to be a key factor in understanding
the transmission dynamics of gastrointestinal parasites in this system.
The focus on the interface between humans and
wild macaques here is especially relevant in light of
three factors. First, macaques are an established
source of infectious zoonotic diseases and carriers of
anthroponotic diseases, including cryptosporidiosis,
giardiasis, and microsporidiosis [Edmonson et al.,
1998; Ekanayake et al., 2006; Engel et al., 2002; Jiang
et al., 2008; Jones‐Engel et al., 2008, 2005, 2004;
McClure et al., 1980; Ye et al., 2012]. Second, previous
work in this system has found intestinal helminthes,
including hookworms, tapeworms (Taenia spp.), and
roundworms (Ascaris spp.), and protozoa, including
Entamoeba spp. and Giardia spp., to be prevalent
across populations [Lane et al., 2011]. These intestinal parasites, and others with similar transmission
strategies, have all been reported in human populations as well, allowing for the opportunity for

continued infection and reinfection to cycle between
macaques and humans [Pederson et al., 2005;
Sutisna et al., 1999]. Finally, and most importantly,
the overlap between humans and macaques, especially concentrated at these monkey forests, has the
potential to exacerbate infection dynamics in these
communities [Fuentes, 2006]. In this study, we
explore how an individual’s attitude towards wildlife,
specifically interactions with non‐human primates,
can impact potential risk of exposure to parasites. To
do this, we investigate how an individual’s age,
occupation, education level, and community of residence correlates with his or her willingness to
participate in exposure risk behaviors, that is, those
behaviors that put an individual in direct contact
with a macaque or macaque feces. We hypothesize
that individuals working directly with macaques,
such as priests or temple staff, the youngest age
group sampled (or those individuals between the ages
15 and 24), and those individuals with the lowest
levels of education will report the greatest participation in exposure risk behaviors. We also investigate
whether increased participation or willingness to

participate in exposure risk behaviors could translate
to increased risk of actual infection via exposure to
gastrointestinal parasites from local macaques. We
hypothesize that if there is a perceived risk of
infection via exposure to macaques, individuals will
be more likely to participate in high levels of exposure
risk behaviors in communities surrounding macaque
populations with the lowest parasite prevalence and
intensity. These behaviors include direct contact with

macaques, recognized and unrecognized water sharing, and pet ownership. Alternatively, if there is no
perceived risk of infection from exposure to macaques, we hypothesize that the relationship between
the incidence of exposure risk behaviors in humans
and parasite loads in macaques will vary randomly
across all communities.
METHODS
Study Sites
Previous studies [Fuentes, 2006; Fuentes et al.,
2005; Lane et al., 2011; Loudon et al., 2006] have
documented 43 temples with well‐established, long‐

term populations of M. fascicularis on the island of
Bali, Indonesia. Native Balinese visitors at 13 of
these monkey forests (Fig. 1) were interviewed
(n ¼ 113) during the summer of 2007. All individuals
asked to participate did so willingly. Interview sites,
described in Table I, were chosen in order to capture
the full range of available habitat type (described as
the amount in m2 of contiguous forest, rice agriculture, and urban areas surrounding each monkey
forest), amounts of foreign tourism (Tourism Days,
defined as the number of days non‐Balinese tourists
were present), and water availability (Water Days,
defined as the number of days in which standing
water is available) [Lane et al., 2011]. Macaque
population size was determined by repeated censuses
from 2002 to 2005 [Fuentes et al., 2005] and via
repeated daily population censuses (n  4 per site
visit). At each site, direct observations were also
made of macaque water use.
Interviewees
Interviews focused on individuals living and
working in or near established monkey forests (Fig.
1). Interviews were opportunistic in that all available
Balinese individuals in the area of the selected
temple, throughout the collection day, were asked
to participate. Both men and women were actively
solicited for participation, and attempts were also
made to include individuals from across a broad
spectrum of age classes, with the exception of
children (Table II). Respondents include farmers,
temple staff, priests, vendors, and local village
members. For the comfort of the interviewees, interviews were conducted, as much as possible, by our
team members who are native Balinese. No tourists
were interviewed for this work [HSIRB Protocol
07‐152.].
Ethnographic Data Collection
Interview questions asked were based on previous successful ethnographic data collections [Loudon
et al., 2006] and were expanded to assess perceptions

Am. J. Primatol.

162 / Lane‐deGraaf et al.

TABLE I. Study Site Details

Population
Padangtegal
Uluwatu
Batur
Angseri
Bedugal
Batupageh
Pulaki
Tejakula
Alas Nengahn
Lempuyang
Bukit Gumang
Mekori
Pejuritan

Population
abbreviation

Number of
interviews

Macaque N

Water days

Tourism days

Forest (m2)

Rice (m2)

Urban (m2)

PU
U
BT
AN
BD
BP
PL
TK
AN
LM
BG
MK
PJ

20
15
4
7
8
7
10
6
9
6
6
12
3

350
300
25
40
200
45
200
75
50
60
100
60
30

244
91
91
244
244
91
244
91
244
365
91
365
244

365
365
244
91
244
91
244
91
365
91
244
91
91

36,002
0
0
536,319
536,319
0
106,198
417,946
510,781
180,053
0
566,899
566,899

807,051
0
0
123,203
0
0
0
114,393
724,907
0
131
298,983
123,203

72,013
23,372
0
102,191
9,473
6,546
87,969
23,372
32,233
127,074
0
87,969
0

Population abbreviation corresponds with map (Fig. 1) detail. Descriptive details (water days, tourism days, forest, rice, and urban) show the number of
available water, frequency of tourists, and type of overall habitat surrounding each site.

related to exposure risk involving macaques. Interviews were conducted in Bahasa Indonesia or Bahasa
Bali, depending on the comfort of the interviewee and
in a manner that encouraged direct answer and
elaboration when appropriate. We limited our investigation to those questions and answers that allowed
us to both understand the nature of risk to parasite
exposure and to avoid highly subjective interpretation of the results. Questions largely focused on
identifying perceptions and behaviors that have been
previously identified to increase the potential for
exposure to the etiological agents of diarrheal
diseases and that addressed the overall risks
associated with direct contact with macaques [Engel
et al., 2002; Jones‐Engel et al. 2004]. With our
questions, we sought to identify the willingness to
participate in risk behaviors associated with overall
attitude toward macaques through direct questioning (i.e., How do you feel about the macaques?) and
indirect questioning (i.e., Do you hunt macaques?).
We also sought to identify the frequency and type of
overlapping water use between people and macaques
and the perceived safeguards or limits to water
sharing. Specifically, we used the designation of
“shared water use” to signify behaviors practiced by

the Balinese that reflected knowingly sharing water
with macaques, such as swimming in the same pool of
water. Alternatively, we used the designation of
“macaque water uses” to indicate behaviors practiced
that reflected unknowingly sharing water with
macaques, such as washing food upstream of the
area frequented by macaques. Water sources for each
monkey temple were the most apparent source of
community‐available water. Uses for shared water
include bathing, drinking, washing, and use as
“sacred water.” Although we used additional questions to gain information regarding potentially taboo
subjects, such as education and income levels in order
to understand how these factors influenced risk
behaviors, questionnaires were designed to minimize
any discomfort caused by these questions. Survey
questions were read to the interviewee to overcome
any potential literacy issues. Answers were recorded
in the language spoken (English, Bahasa Indonesia,
or Bahasa Bali) and were transcribed into English
(for the full set of interview questions, please see
Appendix 1). All collections were approved by the
University of Notre Dame IACUC (protocol 07‐001)
and HSIRB (protocol 07‐152) and the Indonesian
Institute of Science (permit number 662.02/1090.

TABLE II. Numbers of Surveys Collected Total and Relating to Each Category
Age of interviewees
15–24
25–34
35–44
45–54
55–64
65þ
Total

5
28
41
19
16
4
113

Occupation
Priest
Teacher
Laborer
Farmer
Vendor
Temple staff

Education
9
13
17
68
12
6
113

No education
Elementary
Junior high school
High school
Post secondary

Regions were determined by the grouping of macaque populations based on likelihood of corridors for gene flow in the landscape.

Am. J. Primatol.

5
59
24
16
7
113

Behavior and Parasite Exposure Risk / 163

DIII). Our research adhered to the American Society
of Primatology’s principles for the ethical treatment
of primates.
Data Analysis
Information was collected by self‐reporting on
age, education level, occupation, and community/
temple site. Behaviors were labeled as risk behaviors
if they facilitated an exposure through direct contact
with macaques or macaque feces. While we are most
interested in understanding gastrointestinal parasite transmission between overlapping human and
macaque populations, hence our focus on water use,
the survey also provided us an opportunity to explore
the potential risk from other parasites transmitted
via direct contact with macaques by asking participants about their fear of macaques (decreasing
contact) and their level of engagement in hunting
and eating macaques (increasing contact).
Log‐linear analyses were performed, comparing
each category (occupation, education, age, and
temple) to respondents’ answers for fear of macaques,
direct contact with macaques, pet ownership, hunting and eating macaques, sharing water knowingly,
and unrecognized water sharing. Log‐linear analysis
is a backwards hierarchical method that identifies
potential interaction effects, making it ideally suited
for analyzing survey data with yes/no response
variables across multiple categories of explanatory
variables [Vaske, 2008]. An extension of the Pearson’s chi‐square test, log‐linear analysis allows for
the analysis of multiple explanatory variables. Thus,
we were able to identify significant groups of
exposure risk takers with specific targeted survey
answers indicative of attitude toward macaques and
overlapping water use patterns.

RESULTS
Human–Macaque Interactions
While most interviewees (90%) responded that
macaques are “sacred,” or considered components of
the Balinese religious structure in which they reside,
75% of those questioned believe that macaques are
responsible for raiding crops, either their own or
others in their community, 3% of the respondents
admit to eating macaques, and a surprising 12%
admit to hunting macaques, despite widespread social
taboos against hunting. Most respondents reported
positive feelings about the macaques’ presence (81%),
with only 19% reporting a fear of macaques.
Shared Water Consumption
Across the island, 68% of the respondents acknowledge their own shared water use with macaques;
however, many individuals also report using water

frequently and for purposes that would result in
consuming water without recognizing the macaques’
use of water. Balinese were observed washing food
directly in shared water sources at every location, yet
this behavior went unreported entirely. Although not
incorporated directly into the data presented here,
several interviewees acknowledged a risk of infection
from macaques using community water sources and
made efforts to minimize their individual risks by
using “clean” water for specific behaviors (e.g.,
drinking and cooking) upstream of where they believe
macaques use water sources while using water
downstream or “contaminated” water for other behaviors (e.g., bathing and washing). However, these
individual reports were often given while participants
were actively not practicing these behaviors and often
with the acknowledgement that these behaviors were
not practiced community wide. Further, while many
respondents accept the localized view of minimizing
exposure by participating in exposure risk behaviors
only upstream of the perceived source of infection
(i.e., macaques or macaque feces), no single respondent acknowledged the more global, island‐wide
view that locally upstream is systemically downstream of neighboring monkey forests as well as
downstream of neighboring villages and other domesticated and wild animal use. This likely explains the
lack of reports on filtering or boiling water before
consumption.
Exposure Risk Behaviors
Log‐linear analysis of respondents’ reports of fear
of macaques shows a significant overall pattern (x2:
51.95, P ¼ 0.019), suggesting that independent of sub‐
category, respondents report high levels of fear of
macaques. Further, every question examined showed
a significant difference overall in respondents’
answers (direct contact: x2: 77.26, P ¼ 0.0001; pet
ownership: x2: 61.68, P ¼ 0.0018; hunting/eating
macaques: x2: 87.65, P ¼ 0.0001; recognized water
sharing: x2: 84.23, P ¼ 0.0001; macaque water use
(unrecognized): x2: 86.31, P ¼ 0.0001). Scaling down
to compare across education, age, occupation, and
temple, for fear of macaques, direct contact, shared
water, and macaque water use, temple is the only
significant explanatory variable (fear of macaques:
x2: 21.72, P ¼ 0.041; direct contact: x2: 44.69,
P ¼ 0.0001; shared water: x2: 56.12, P ¼ 0.0001;
macaque water use: x2: 36.88, P ¼ 0.0002), suggesting
that for these questions, the most important factor
determining a respondents’ willingness to participate
in these exposure risk behaviors is the community
temple into which they were born. However, willingness to own pets and to hunt and eat macaques had
an additional explanatory variable. Both temple and
level of education were significant in explaining
patterns of pet ownership (temple: x2: 35.46,
P ¼ 0.0004; pet ownership: x2: 12.91, P ¼ 0.012), while

Am. J. Primatol.

164 / Lane‐deGraaf et al.

temple and age were significant factors explaining
willingness to hunt and eat macaques (temple: x2:
63.51, P ¼ 0.0001; age class: x2: 31.77, P ¼ 0.0004).
Within category analyses (i.e., across age classes
or occupations), we found no significant differences
among any group’s response to fear of macaques.
However, community temple and at least one other
category had a subgroup that showed a significantly
higher or lower willingness to participate in exposure
risk behaviors for all other response categories. For
direct contact and pet ownership, both temples and
occupation had subgroups with significant explanatory variables. Two temples (AS and MK) had significantly lower contact rates, while one temple (PU)
had significantly greater contact rates (x2: 42.93,
P ¼ 0.0001). One temple (TK) had significantly
greater reports of pet ownership, while one temple
(MK) had significantly fewer reports of pet ownership
(x2: 29.37, P ¼ 0.0002). Perhaps not surprisingly,
temple staff reported significantly greater rates of
contact while individuals in the education field
(teachers and students) reported overall significantly
lower rates of direct contact with macaques (x2: 11.31,
P ¼ 0.047). However, individuals in the education
field reported significantly greater amounts of pet
ownership; farmers reported significantly lower levels
of pet ownership (x2: 13.83, P ¼ 0.038). Two categories
—temple and age class—had significant explanatory
subgroups for reports of hunting and eating macaques. Two temples (BT and PL) and two age classes
(20–24 and 60–64) had a significantly greater number
of reports of hunting and eating macaques (temples:
x2: 27.21, P ¼ 0.0043; age classes: x2: 18.68,
P ¼ 0.0031). Finally, for both metrics of water
sharing—shared use (recognized) and macaque use
(unrecognized)—temple and education level had
significant explanatory subgroups. Two temples had
significantly lower reports of both shared water use
and macaque water use (BD and MK); one additional
temple (BT) had significantly lower reports of shared
water use (shared water use: x2: 47.31, P ¼ 0.0001;
macaque water use: x2: 70.32, P ¼ 0.0001). Only one
education class showed a significant explanatory
relationship with water use—no education. Individuals with no education reported significantly lower
levels of both shared water use and macaque water
use (shared water use: x2: 17.84, P ¼ 0.009; macaque
water use: x2: 21.97, P ¼ 0.0002).
DISCUSSION
Our results demonstrate the people living in and
around Balinese monkey forests participate in exposure risk behaviors. Most significantly, community
temple was a significant explanatory variable for
every question of interest and was the only significant
explanatory variable in the case of reports of fear of
macaques, direct contact, and both types of shared
water uses.

Am. J. Primatol.

We hypothesized that fear of macaques would
result in fewer direct interactions with macaques.
However, we found that temple site was the only
explanatory variable, island wide, for reports of fear of
macaques. This could be explained by personal stories
shared between community members and suggests
that individually reported attitudes toward macaques are not separable from an individual’s home
temple as an important determinant in the willingness to participate in exposure risk behaviors. Direct
contact with macaques was hypothesized to be higher
among the young, the uneducated, and those with
occupations that place them at temple sites directly.
We found that the temple staff reports the greatest
amount of direct contact with macaques. With 100% of
temple staff reporting frequent direct contact with
macaques while other groups report significantly less,
the disparity between the views of temple staff and
other individuals, including temple priests, likely
reflects additional, underlying demographic and
social factors, such as social position and the role
staff play in the temples. We also found that
individuals at PU reported the greatest amount of
direct contact with macaques. This temple is home to
the largest macaque population on the island, with
recent estimates nearing 600 macaques [Brotcorne
et al., 2011]. It is also the temple with the most
international tourism, greatest amounts of provisioning, and most organized management staff. Thus, it is
especially important when considering the risk of
exposure to parasites. For example, Jones‐Engel et al.
(2008) documented transmission of SFV from macaques to individuals working in a monkey forest,
suggesting transmission has already and will continue to occur between humans and macaques at these
temples.
Ownership of non‐human primates as pets is
common throughout Bali, and throughout rural
regions of Indonesia. There exists a disparity
between what individuals consider direct contact
associated with risk (e.g., bites and scratches) and
other types of direct contact (e.g., sharing living
quarters), despite the opportunity of parasite exposure from this latter category as well. Both temple
site and education level were significant predictors of
pet ownership, with the temple TK and those in the
education field reporting the greatest amount of pet
macaques within these subgroups. Thus, those in the
education field report the greatest amount of pet
ownership while concurrently reporting the least
amount of direct contact with macaques, suggesting
that pet macaques are considered a special case of
contact to these individuals.
There is both a social and religious taboo against
hunting and eating macaques on Bali, and it is likely
that this practice was under‐reported. Despite these
taboos, both age and temple site were significant
explanatory variables of willingness to hunt and eat
macaques. The two populations—BT and PL—that

Behavior and Parasite Exposure Risk / 165

report the greatest amount of these exposure risk
behaviors are both dry and difficult terrain in
relatively impoverished areas of the island, possibly
making hunting an attractive option in order to
supplement an individual’s diet. Also, two specific age
groups—15 to 24 and 55 to 64 report the greatest
amount of hunting and eating macaques. Overall,
while the risk of parasite transmission is generally
greatest from hunting and eating macaques, through
exposure to potentially infective blood, intestinal
system, muscle, and brain matter [Wolfe et al., 2005],
these behaviors contribute a small, yet significant,
exposure risk to the subset of the Balinese population
engaging in these practices [Wolfe et al., 1998, 2005].
Gastrointestinal parasites infect 1 billion people,
and most of these parasites are water‐ and soil‐borne
parasites [Alum et al., 2010; Stepek et al., 2006].
Thus, it was surprising to discover that most Balinese
do not recognize the extent of overlap in water use
patterns between themselves and the wildlife with
which they share the island. Despite the recognition
that macaques use community water sources, the
prevalence of recognized shared water use within the
overall Balinese community structure is low, with
those with no education reporting significantly lower
levels of recognized shared water use. Given the
recent programs in Balinese schools focused on clean
water, this low level of recognized shared water use is
surprising and has ramifications in potentially
increasing parasite transmission opportunities. Coupled with the high levels of unrecognized macaque
water use, this trend of water use throughout Bali can
substantially contribute to the spread of parasites,
specifically gastrointestinal parasites, throughout
the island.
While all temples are known to have a gastrointesntial parasite burden, previous work has shown
that the temples AS, TK, LM, and PU have
significantly greater gut parasite burden and BD,
MK, U, and AN have significantly lower gut parasite
burden than surrounding macaque populations
[Lane et al., 2011]. This increase or decrease in
gastrointestinal parasite burden at these populations
has been shown previously to be associated with
amount of anthropogenic land use in the surrounding
communities. Interestingly, five of these temples—
BD, MK, AS, TK, and PU—also showed a significant
reporting of at least one exposure risk behavior.
Thus, it is these communities that are of particular
interest for understanding the relationship between
actual and perceived risk of exposure to gastrointestinal parasites from local macaques. For example,
two populations—BD and MK—previously found to
have low parasite burden co‐occur with significantly
lower levels of reported shared water use and
macaque water use, as well as significantly lower
levels of reported pet ownership and direct contact in
MK. As such, individuals in these communities, even
when participating in exposure risk behaviors, are

unlikely to become infected with gut parasites
originating with macaques. One population—AS—
previously found to have a high parasite burden co‐
occurred with significant decreases in reports of
direct contact, suggesting that while individuals in
this community rarely participate in exposure risk
behaviors, when they do, the risk of infection is great.
Finally, two communities—TK and PU—were previously shown to have a high parasite burden and were
found to have a significant increase in either pet
ownership (TK) or direct contact (PU). As a result,
individuals in these communities are at a real risk of
becoming infected with gastrointestinal parasites,
originating with macaque populations, via either
direct contact or pet ownership. In summary, our
results show that the willingness to participate in
exposure risk behaviors of the Balinese is largely
context specific and varies most by community,
independent of the actual exposure risk to gut
parasites from macaque populations. Therefore, local
cultural and demographic factors are likely more
important in determining participation in exposure
risk behaviors in the context of local macaques much
more so than actual parasite burdens carried by those
macaques.
Understanding the demographic patterns influencing exposure to parasites is an important component of minimizing transmission opportunities.
While this research focuses directly on risk parameters on the island of Bali with an emphasis on risk
associated with long‐tailed macaques, we demonstrate that human socioeconomic factors can influence specific behaviors, which, in the context of wild
primate populations, may affect the risk of exposure
to infectious agents. While this is significant for
diarrheal diseases due to their clear environmental
transmission strategies, this knowledge is also
important for understanding the overarching role of
the anthropogenic environment in opportunities for
infectious disease transmission and emergence more
generally.
ACKNOWLEDGMENTS
The authors would like to thank Concerta Holley
and Robert Plasschaert for assistance with data and
for helpful discussion of the manuscript. Funding for
this work was provided by the National Science
Foundation (BSC‐0639787) and by the University of
Notre Dame’s Institute for Scholarship in the Liberal
Arts. HSIRB [Protocol 07‐152] was granted for the
human portion of this work, and IACUC [Protocol 07‐
001] was granted for the parasite portion.
Appendix 1
1. How long have you and/or your family lived in
this area?

Am. J. Primatol.

166 / Lane‐deGraaf et al.

2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
28.
29.
30.
31.
32.
33.
34.
35.
36.

What is your profession?
What is your level of education?
What is your religious affiliation?
How often do you visit a temple?
Do macaques frequent this temple? If so, how
often?
How often does you family use the temple
associated with macaques?
What is the origin of the macaques at this
temple?
How do you feel about the macaques? Is this
feeling shared by all members of your family?
How does it differ?
Do others in your village have a different view of
the macaques than you?
Where do the macaques live?
How many macaques come to this place?
Are the macaques sacred?
Do you have direct contact with the macaques?
What kind?
Do you pester the macaques? How? How often?
Do the macaques at this site raid your crops? How
often and when?
How do you deter the macaques from coming to
the temple or raiding your fields?
Have you ever been injured by a macaque?
Have you seen any dead macaques here?
Does anyone keep macaques as pets?
Do the macaques eat trash?
Do you eat the macaques?
Do you hunt the macaques for any reason?
Are you afraid of the macaques?
Do you think there will be a change in the way
people perceive macaques here?
Have you seen the macaques using rivers,
irrigation channels, or sawah?
How often do macaques use the water?
How often do they use the water sources here?
How does your village use the water?
How often does your village use the water here?
Has there been a change in water use in reference
to the macaques?
Do you share a water source with the macaques?
How do you use this shared water?
How do the macaques use this water?
Where do the macaques drink from?
Have you seen the macaques swim?

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