Download Black and gold howler monkeys (Alouatta caraya) as sentinels of

American Journal of Primatology 73:75–83 (2011)
RESEARCH ARTICLE
Black and Gold Howler Monkeys (Alouatta caraya) as Sentinels of Ecosystem
Health: Patterns of Zoonotic Protozoa Infection Relative to Degree
of Human–Primate Contact
MARTIN M. KOWALEWSKI1, JOHANNA S. SALZER2, JOSEPH C. DEUTSCH3, MARIANA RAÑO1,
MARK S. KUHLENSCHMIDT3, AND THOMAS R. GILLESPIE2,4
1
Estación Biológica de Usos Múltiples de Corrientes (EBCo), Museo Argentino de Ciencias Naturales-CONICET, Argentina
2
Department of Environmental Studies and Program in Population Biology, Ecology, and Evolution, Emory University,
Atlanta, Georgia
3
Department of Pathobiology, College of Veterinary Medicine, University of Illinois, Urbana, Illinois
4
Department of Environmental and Occupational Health, Rollins School of Public Health, Emory University, Atlanta, Georgia
Exponential expansion of human populations and human activities within primate habitats has
resulted in high potential for pathogen exchange creating challenges for biodiversity conservation and
global health. Under such conditions, resilient habitat generalists such as black and gold howler
monkeys (Alouatta caraya) may act as effective sentinels to overall ecosystem health and alert us to
impending epidemics in the human population. To better understand this potential, we examined
noninvasively collected fecal samples from black and gold howler monkeys from remote, rural, and
village populations in Northern Argentina. We examined all samples (n 5 90) for the zoonotic protozoa
Cryptosporidium sp. and Giardia sp. via immunofluorescent antibody (IFA) detection. All samples were
negative for Cryptosporidium sp. The prevalence of Giardia sp. was significantly higher at the rural site
(67%) compared with the remote forest (57%) and village (40%) sites. A lack of Cryptosporidium sp. in
all samples examined suggests that this pathogen is not a natural component of the howler parasite
communities at these sites and that current land-use patterns and livestock contact are not exposing
Argentine howler monkeys to this pathogen. High prevalence of Giardia sp. at all sites suggests that
howler monkeys may serve as a viable reservoir for Giardia. Significantly higher prevalence of Giardia
sp. at the rural site, where primate–livestock contact is highest, suggests the presence of multiple
Giardia clades or increased exposure to Giardia through repeated zoonotic transmission among
nonhuman primates, livestock, and/or people. These results highlight the need for future research into
the epidemiology, cross-species transmission ecology, and clinical consequences of Giardia and other
infectious agents not only in humans and livestock, but also in the wild animals that share their
environments. Am. J. Primatol. 73:75–83, 2011.
r 2010 Wiley-Liss, Inc.
Key words: Cryptosporidium; disturbance ecology; Giardia; neglected pathogens; primate; Zoonoses
INTRODUCTION
Exponential expansion of human populations
and human activities within primate habitats has
resulted in high potential for multi-directional
pathogen exchange creating challenges for biodiversity conservation and global health [Gillespie et al.,
2008]. Associated landscape-level disturbance may
exacerbate pathogen transmission by affecting the
distribution and behavior of primates [Gillespie &
Chapman, 2006, 2008; Gillespie et al., 2005; Nunn &
Altizer, 2006], as well as vectors of infectious diseases
such as yellow fever, dengue, and malaria [Altizer
et al., 2006; Hay et al., 2002]. In this regard, studies of
nonhuman primates with the ability to survive in
moderately disturbed habitats are of great importance for understanding the dynamics of infectious
disease transmission and to evaluate the capacity of
r 2010 Wiley-Liss, Inc.
primates to serve as sentinels, alerting us before
pathogens reach semi-urban or urban areas.
The forests of Northern Argentina provide an
ideal locale for examining issues related to pathogen
exchange between people, nonhuman primates, and
Contract grant sponsor: NIH; Contract grant number: T35 2006;
Contract grant sponsors: The Wenner Gren Foundation; PostPh.D. Research Grant; Contract grant number: 7622; Contract
grant sponsor: Conservation Medicine Center of Chicago.
Correspondence to: Thomas R. Gillespie, E510 Math and
Science Center, 400 Dowman Drive, Emory University, Atlanta,
Georgia 30322. E-mail: [email protected]
Received 28 September 2009; revised 26 December 2009;
revision accepted 26 December 2009
DOI 10.1002/ajp.20803
Published online 18 January 2010 in Wiley Online Library (wiley
onlinelibrary.com).
76 / Kowalewski et al.
livestock. Here, commercial agriculture (i.e., soy
plantations) and forest exploitation have profoundly
changed the composition of forests, eliminating the
hardiest and most economically profitable forest tree
species [Zunino & Kowalewski, 2008]. Clearing
entire forests for agriculture and establishing exotic,
fast-growing pastures are also contributing to rapid
landscape change in this region. The effects of these
changes on wildlife populations remain largely
unknown. In Argentina, black and gold howler
monkeys, Alouatta caraya, account for the highest
proportion of biomass of arboreal mammals and
these monkeys often cope well with moderate
deforestation [Zunino et al., 2007]. The high degree
of phenotypic plasticity present in this species make
black and gold howler monkeys a valuable species to
test and evaluate current ideas of conservation
related to the dynamics of emergent and re-emergent
diseases [Kowalewski & Gillespie, 2009], since more
plastic species are expected to occupy and successfully exploit a wider range of ecological conditions,
leading to greater resilience to habitat seasonality
and habitat modification compared with other taxa
[Miner et al., 2005]. Howlers are classified as
colonizers [Crockett, 1998; Crockett & Eisenberg,
1987; Eisenberg et al., 1972] due to their ability to
adapt and survive in modified environments [BiccaMarques, 2003; Clarke et al., 2002a]. This ability
to survive in variable environments including habitats that bring them into contact with humans
[Cabral et al., 2005; Estrada et al., 2006; Muñoz
et al., 2006] or increase their terrestrial travel
[Kowalewski et al., 1995; Pozo-Montuy & SerioSilva, 2006; Young, 1981], make howlers an excellent
model to study the dynamics of infectious disease
transmission among wild primates, humans, and
domestic animals.
Although black and gold howlers, much like
other species of Alouatta, seem to be resilient to
variable levels of habitat degradation in terms of
population numbers [Estrada et al., 2006; Zunino
et al., 2007], a finer-scale analysis reveals a different
scenario. As in colobine species [Gillespie & Chapman,
2006, 2008], howler populations living in fragmented
forests seem to be carrying a more diverse community of parasites [Kowalewski & Gillespie, unpublished data; Santa Cruz et al., 2000]. Oklander [2007]
revealed another trend in howler populations living
in fragmented forests in Northern Argentina (the
same study site of this article—EBCo-, see description in methods). Oklander [2007] used molecular
techniques [13 polymorphic microsatellites developed by Oklander et al., 2007] to compare levels of
homozygosity in a population living in a continuous
forest and a population living in a fragmented forest
(same rural population studied in this article) by
estimating gene flow with Fst values. In contrast to
groups living in continuous forests (our IB site, see
methods), groups living in fragments presented a
Am. J. Primatol.
recent genetic differentiation among groups and a
lower genetic heterozygosity, potentially due to
limitations in dispersal opportunities [Oklander,
2007]. The impacts of habitat alteration on nonhuman primate populations occur at the individual,
group, and population level. Successful mediation of
these threats requires repeated evaluation of genetic
diversity, health, stress, behavior, and diet. A study
on red colobus (Piliocolobus tephrosceles) revealed
the synergistic affects of food availability, cortisol
levels, and parasite infections on the abundance of
this species [Chapman et al., 2006]. Case studies of
various species from sites around the world will
improve our understanding of the multifactorial
process that anthropogenic disturbances can initiate
at different levels.
In this study we examine patterns of infection
with the zoonotic protozoa, Giardia, and Cryptosporidium, in populations of black and gold howler
monkeys living at variable levels of contact with
humans: remote, rural, and village. These protozoa
infect vertebrates, including wildlife, livestock, and
humans [Hill, 2001; McGlade et al., 2003; Volotão
et al., 2008]. The protozoa life cycle consists of
fecal–oral transmission of Giardia cysts or Cryptosporidium oocysts (infective stage), typically via
contaminated water and food. Within the host
animal, the life cycle of the protozoa continues as
the cysts or oocysts develop into trophozoites. The
trophozoites infect cells within an animal host’s
duodenum; often leading to severe diarrhea [Thompson,
2004]. Giardia is cosmopolitan and constitutes a
recognized waterborne infection for humans and
animals, responsible for well over one billion cases of
human diarrheal disease annually [Crompton, 2000;
Teodorovic et al., 2007; WHO/UNICEF, 2000].
Giardiasis is now considered by the World Health
Organization to be a ‘‘neglected disease,’’ due to its
ubiquity in equatorial latitudes, its chronic detrimental health effects (especially in children), its
propensity to infect economically disadvantaged
populations, and the paradoxical availability of
relatively inexpensive and effective pharmaceuticals
for its treatment [Savioli et al., 2006]. In Latin
America almost 15% of the rural population is
infected with Giardia [Atı́as, 1999]. In Argentina,
two human studies showed a prevalence of 10% in
urban areas, 34% in small towns (same as villages
considered in our study) [Gamboa et al., 2003], and
4% in rural areas [Minvielle et al., 2004]. In animals
from this region the reported prevalence of Giardia
is 7.5% in cattle, 18.6% in dogs, and 3.9% in rodents
[Pezzani et al., 2003]. These parasites have been
reported in other nonhuman primates including
mountain gorillas (Gorilla gorilla berengei) [Graczyk
et al., 2002], black howler monkeys (Alouatta pigra)
[Vitazkova & Wade, 2006], brown howling monkey
(Alouatta guariba) [Cabral et al., 2005; Volotão et al.,
2008], red colobus (Pilocolobus tephrosceles) [Salzer
Howler Monkeys as Sentinels for Conservation and Health / 77
et al., 2007] and red-tailed guenons (Cercopithecus
ascanius) [Salzer et al., 2007]. As evidenced from the
examples above, giardiasis is often endemic in
human populations; however, the frequency and
pathogenicity of this agent remains largely unknown
in wildlife [Appelbee et al., 2005; Levy et al., 1998].
The main symptoms of giardiasis in humans are
diarrhea, abdominal pain, nausea, and vomiting
[Acha & Szyfres, 2003]. The disease is generally
described as an acute diarrheal illness that may last
up to six weeks although chronic patients are also
found, especially in cases of impaired immunocompetence [Chester et al., 1985].
METHODS
Study Sites
This study was conducted in four sites that
differ in their degree of human use: Isla Brasilera
(IB) (271200 S, 581400 W), Estación Biológica Corrientes-Biological Field Station Corrientes- (EBCO)
(271300 S, 581410 W), Cerrito (C) (271170 S, 581370 W),
and San Cayetano (SC) (271340 S, 581420 W) (Fig. 1).
IB is an island characterized by a continuous flooded
forest where howler groups exhibit extensive home
range overlap, but little to no human contact. The
island has an area of 290 ha and we have identified
between 32–35 groups. IB is 20 km north of EBCO
(Fig. 1), a rural site characterized by semi-deciduous
forest surrounded by a matrix of grassland. At
EBCO, in general there is one group of howlers per
forest fragment. We have identified 34 groups of
howlers in 24 forest fragments (area from 3 ha to
approximately 30 ha) covering a total area of 3,000 ha
[see Zunino et al., 2007 for details]. This site is under
continuous deforestation due to selective logging and
clearing of fragments for cattle ranches and howlers
have the potential of close contact with cattle, other
domestic animals, and humans when accessing
shared water sources and during terrestrial travel.
Terrestrial travel is typical of other howler populations living in similar conditions [Clarke et al.,
2002b; Glander, 1992; Horwich & Lyon, 1998;
Pozo-Montuy & Serio-Silva, 2006]. Human houses
are distributed uniformly across this rural site. We
also sampled howlers from two village sites, Cerrito
town (C) near IB (there are two groups of howlers
living in this town of 1,500 human inhabitants) and
SC next to the EBCO with almost 4,000 human
inhabitants (there are 7–8 groups living in close
proximity with family houses whose tree crowns are
contiguous with trees in the forest fragments). In
summary, the four areas were classified into three
habitat types: remote (IB), rural (EBCO), and village
(C and SC). The climate of all sites is subtropical
with an average annual temperature of 21.61C and
an annual average of rainfall of 1,200 mm [Rumiz
et al., 1986]. Rains increase slightly towards the
spring–summer (September to December).
Study Population
We collected 90 fecal samples from different
individuals during March 2008 (fall season): 30
samples from the village sites (C and SC), 30 samples
from the rural site (EBCO) and 30 samples from the
Fig. 1. Location of study areas of black and gold howler monkeys (Alouatta caraya) in northern Argentina: San Cayetano (SC) and
Cerrito (C) were considered village sites, Isla Brasilera (IB) a remote site, and EBCO a rural site.
Am. J. Primatol.
78 / Kowalewski et al.
remote site (IB). Each sample set consisted of 30
samples and included 10 adult males, 10 adult
females, 4 adult females with lactating infants, and
approximately 3 juvenile males and 3 juvenile
females (the number of juveniles varied across
groups). These samples were collected from different
groups of howlers in each site.
Sample Analysis
Fecal samples were collected immediately after
defecation in (March 2008) and preserved in 10%
neutral buffered formalin [Gillespie, 2006]. When
collected, fecal consistency was characterized as
liquid, soft, medium, or solid. We used a Merifluor
Cryptosporidium/Giardia Direct Immunofluorescent
Detection Kit (Meridian Bioscience Inc, Cincinnati,
Ohio) to detect both parasites of interest—Crystoporidium oocysts and Giardia cysts based on monoclonal antibodies [Johnston et al., 2003]. The
analysis was run in July 2008. Fecal samples were
scored both for the presence or absence of the
pathogens as well as quantification of Cryptosporidium oocysts and Giardia cysts in feces. Fecal
samples were concentrated and then resuspended
in 1 g/1 mL suspensions. Counts were calculated by
analyzing 10 mL of the 1 g/mL solution of concentrated feces from each sample. Oocysts or cysts were
then quantified by counting total numbers in 150
microscope fields (400 magnification) and extrapolating results to the entire sample. This method
was validated by spiking negative fecal samples with
known numbers of Cryptosporidium sp. oocysts.
Statistical Analyses
Differences in the frequency and prevalence of
infections across sites and differences in frequencies
of fecal consistency were compared using w2 tests. We
used Kruskall Wallis ANOVA to explore differences
of intensity of infection across sites. We considered a
criterion for significance for all statistical tests at
Po0.05. This research complied with the American
Journal of Primatology and University of Illinois
guidelines for the ethical treatment of primates
(IACUC protocol 06207) and the laws of Argentina.
RESULTS
All samples were negative for Cryptosporidium
sp. Seventeen of 30 samples (57%) in the remote site,
20 of 30 samples (67%) in the rural area, and 12 of 30
samples (40%) in the village areas were positive for
Giardia sp. When the remote, rural, and village sites
were compared collectively, the prevalence of Giardia
sp. infection in black and gold howler monkeys was
not significantly related to the location of sampling
(w2 test, df 5 2, P>0.05). When sampling locations
were compared individually (remote vs. village,
rural vs. village, and remote vs. rural), significant
Am. J. Primatol.
Fig. 2. Giardia sp. cysts/gram in black and gold howler monkey
(Alouatta caraya) feces from remote, rural, and urban sites in
northern Argentina.
differences were found between rural and village
areas (w2 test, df 5 1, Po0.03). No fecal samples were
scored as liquid. From a total of 49 positive samples,
15 (31%) were characterized as soft, 27 (55%) as
medium and 7 (14%) as solid. These results suggest
that the consistency of fecal material is independent
of the infected state of the individuals (w2 test, df 5 2,
Po0.05).
We also compared cysts per gram of fecal
material, providing an index of intensity of shedding
and environmental contamination with Giardia.
Although the mean value of cysts per gram was
highest in remote areas (250.9, range 5 4–1,064),
followed by village areas (194.7, range 5 1–790) and
rural areas (113.5, range 5 1–845); there were no
significant differences in the relative number of cysts
per sample across areas (Kruskall Wallis ANOVA,
H ¼2ðN¼49Þ ¼3, P40.05) (Fig. 2).
DISCUSSION
Our results demonstrate that Giardia sp. is
present and prevalent in wild black and gold howlers
at all points along a gradient of anthropogenic
disturbance. In these same populations, there is no
evidence of infection with Cryptosporidium sp. A lack
of Cryptosporidium sp. in all samples examined
suggests this pathogen is not a natural component
of the howler parasite communities at these sites and
that current land-use patterns are not exposing
Argentine howler monkeys to this pathogen. Cryptosporidium oocysts were found in people in urban
and semi-urban populations close to our study sites
[Ledesma et al., 2006], but it was never reported for
the rural area considered in this article [Borda et al.,
1996].
High prevalence of Giardia sp. at all sites
regardless of human–primate contact rates suggest
that howler monkeys may serve as a viable reservoir
Howler Monkeys as Sentinels for Conservation and Health / 79
for Giardia sp. Considered among the most common
human intestinal protozoa, Giardia ranges in clinical
presentation from asymptomatic to highly pathogenic, causing chronic malabsorptive diarrhea in
some patients [Thompson, 2004]. Both host factors
(e.g., nutrition, immunity, co-infection with other
agents) and pathogen factors (e.g., strain, infectious
dose) are thought to contribute to the severity of
clinical disease [Thompson, 2000]. In our study, we
did not characterize any howler monkey fecal
samples as liquid, however; we did find that infected
animals had more fecal samples scored as soft and/or
medium than noninfected animals. The lack of a
strong measurable association between infection and
an acute gastrointestinal symptom (i.e., diarrhea) in
our study population was surprising, but it is
concordant with recent studies of humans. Although
Giardia is associated with clinical disease in developed economies, evidence is nevertheless mounting
that it may be commensal in rural settings where
people may normally be exposed to diverse parasite
communities from an early age. For example, Cordón
et al. [2008] found Giardia at 28.1% prevalence in
diarrheic Peruvian children, as well as in 19.5% of
nondiarrheic children, emphasizing the importance
of asymptomatic patients in Giardia transmission
where hygiene and sanitation are poor [Cordón et al.,
2008]. Other studies in India [Traub et al., 2003],
Ethiopia [Ayalew et al., 2008], Bangladesh [Dib et al.,
2008], and Peru [Hollm-Delgado et al., 2008] have
found similarly weak or nonexistent associations
between G. duodenalis infection status and gastrointestinal symptoms, suggesting that G. duodenalis
may coexist benignly with human hosts under
conditions where acquired immunity to the pathogen
can develop. Lack of early exposure and acquired
immunity to G. duodenalis may, in fact, account for
the role of the pathogen as a cause of sporadic
diarrheal outbreaks in developed countries [Istre
et al., 1984], as well as a major cause of traveler’s
diarrhea for people from developed countries who visit
endemic areas [Reinthaler et al., 1998; Shlim et al.,
1999]. The interplay between clinical symptoms and
Giardia infections in wildlife are far less known. We
hope to explore the association between symptom and
infection in black and gold howler monkeys and other
wildlife species in more detail in future work.
Giardia is also notable for zoonotic transmission
[Thompson, 2004]. The protozoan’s propensity to
cross species barriers results from the host nonspecificity of the trophozoite as well as from the high
infectivity and environmental stability of the Giardia cyst [Smith & Nichols, 2006]. The fact that
Giardia sp. prevalence was significantly higher at
the rural site in our study, where monkeys have the
highest contact rates with cattle and other domestic
animals, suggests that repeated zoonotic transmission may amplify baseline rates of infection [Zunino
& Kowalewski, 2008].
There are several reasons to expect higher rates
of contact between howlers and cattle, a common
source of protozoal zoonotics, in this rural site. First,
cattle routinely enter forest fragments inhabited by
howlers looking for shade and young pastures,
opening trails and defecating along them. Second,
howlers drink water from creeks where cattle drink
and defecate [Kowalewski & Raño, personal observation]. Finally, increased levels of deforestation
decrease the size of these fragments and obligate
howlers to descend to cross from fragment to
fragment looking for food resources [Zunino et al.,
2007] increasing the likelihood of contact with
parasites on the ground and in small water bodies.
As in the case of the rural site, we also found
high prevalence of Giardia in howler populations in
the two other sites (remote and village). Giardia had
a prevalence of 57% in the remote site. Although this
site lacks permanent human settlements, there are
occasional visitors from neighboring towns that
bring a limited number (10–20) of cattle onto the
island, which drink from the same lagoons that the
monkeys use as a water source [Bravo & Sallenave,
2003; Kowalewski, 2007]. Giardia duodenalis was
reported in brown howling monkeys (Alouatta
guariba), as the result of contact of these monkeys
with other wildlife, such as opossums, which live in a
nearby forest fragment and circulate near human
dwellings [Muller et al., 2000; Volotão et al., 2007] or
contact with humans such as fishermen, poachers, or
researchers [Volotão et al., 2007; see also Vitazkova
& Wade, 2007]. Similarly, intensified gorilla–human
interaction has been suggested to enhance transmission of anthropogenic pathogens including Giardia
[see Graczyk et al., 2001a,b, 2002; Nizeyi et al.,
1999].
Although the village site in our study revealed
the lowest prevalence of Giardia (40%), this value is
high relative to Giardia prevalence in other wild
primate populations examined. A study in 1983 of
children from the public school at this site (SC)
showed a 29% (n 5 60) prevalence of Giardia lambia
(5 Giardia duodenalis) infection [Borda et al., 1996].
The interactive affects of poverty, low levels of
education, unsanitary conditions, and increased
levels of deforestation experienced at this site may
result in increased contact between wildlife and
humans, producing unexpected results in the transmission patterns of infectious diseases.
Vitazkova and Wade [2007] suggested a positive
relationship between primate density and prevalence
of Giardia sp. in a population of Alouatta pigra
during the dry season in Belize and Mexico. In our
study, we find the opposite trend with highest
prevalence at the site with the lowest primate
density (1.04 howlers/ha for the rural site) and
lowest prevalence at the site with the highest
primate density (3.25 howlers/ha for the remote site)
[Kowalewski & Zunino, 2004; Zunino et al., 2007].
Am. J. Primatol.
80 / Kowalewski et al.
This pattern suggests that other factors associated
with anthropogenic disturbance such as physical
characteristics of sites (humidity, water availability),
history of both parasites and hosts in sites, variation
in the use of space, and stress may trump host
density in driving patterns of infection with directly
transmitted pathogens.
Black and gold howlers living in fragmented
areas have shown a higher diversity of gastrointestinal parasites [Kowalewski & Gillespie, unpublished
data] potentially due to an increase in contact with
cattle, domestic animals, and humans. In addition, a
study carried out at the same rural site has shown
that howlers have higher levels of homozygosity than
in areas remote from human occupations with
continuous forests [Oklander, 2007; Oklander et al.,
2007]. Collectively, this suggests that howlers are
viable sentinels for overall ecosystem health. For
example, in 2007, an outbreak of yellow fever
decimated the population of A. caraya and A. guariba
in the Province of Misiones (Argentina) located
north of the field sites of the current study [Agostini
et al., 2008; Holzmann, personal communication].
This outbreak also affected humans in the area. In
2008, one year after these reports were made, we
found dead howlers (A. caraya) in the same province
(Corrientes) that likely succumbed to yellow fever
near our study site. Unfortunately, supplies were not
available to allow for diagnostic confirmation. The
yellow fever wave is progressing to the South of
Argentina. Howler deaths constitute an important
signal of an impending public health threat that can
alert officials of the need to intervene to block
conversion of a sylvatic (i.e., forest cycle) into an
urban cycle of this deadly human disease. Black and
gold howlers are effective sentinels of yellow fever,
and ongoing study of their populations may help us
to prevent and better understand the yellow fever
transmission dynamics. Beyond the case of yellow
fever, resilient habitat generalists such as the black
and gold howlers can act as effective sentinels of
overall ecosystem health and alert us to impending
epidemics in human populations. Consequently, we
view the results of this study as indicating a strong
need for future research into the epidemiology, crossspecies transmission ecology, and clinical consequences of Giardia and other infectious agents not
only in humans and livestock, but also in the wild
animals that share their environments.
Recommendations
Successful outcomes involving emerging and
remerging infectious diseases require a proactive
approach, ideally avoiding introduction of infectious
agents into human, livestock, and threatened
wildlife populations altogether. Consequently, surveillance efforts need to be strongest in areas of
increasing contact between humans and wildlife and
Am. J. Primatol.
in poverty-stricken communities where health systems are inadequate. Our study is an illustration of
how these exploratory evaluations may benefit these
efforts. Establishment of long-term study sites allow
researchers to catalog rare events and build knowledge and collaborations over time to better understand the dynamics of infectious diseases and to
potentially prevent future outbreaks. For example,
data presented in this article are part of a long-term
and ongoing study of ecosystem health in northern
Argentina, which includes an evaluation of several
pathogens in humans, domesticated animals and
nonhuman primates among other wild mammals. In
addition to incorporating government institutions
and public universities, our data collection and
sampling design allows the comparison of our results
with similar projects carried out using standardized
methods around the globe [Gillespie, 2006; Gillespie
et al., 2008]. Impoverished people with limited access
to basic hygienic services or adequate health systems
are often most susceptible to emerging diseases.
These same people and wildlife that live in surrounding habitats are often the most affected by the
negative consequences of large-scale habitat modifications, despite being rarely responsible for such
habitat modification [Alarcón-Cháires, 2006]. Local
and national governments must invest resources in
development for such communities in terms of
education, health, and conservation programs and
hold large local landowners and international corporations that produce the highest impact on wildlife
through the establishment of pastures and largescale plantations of soy, oil palm, rice, and other
global agricultural commodities accountable for their
impacts on human, animal, and ecosystem health
[De la Cruz, 2004; Martı́nez Alier, 2005].
Researchers can play an important role in
conservation and development that extends far
beyond the dissemination of results through international scientific journals. They can expand their
capacity by assembling multidisciplinary teams for
conservation and health applications, establishing
education programs that incorporate local people and
researchers in areas of study, and conveying information to local communities through radio, newspaper, and community meetings. Most importantly,
researchers can help colleagues and students in
developing countries to obtain training and funding
for ongoing and proposed research.
Our current knowledge regarding wild primate
pathogens remains minimal and skewed toward
regions of long-term primate research. Fortunately,
integration of standardized empirical data collection,
state-of-the-art diagnostics, and the comparative
approach offers the opportunity to create a baseline
for patterns of infection in wild primate populations;
to better understand the role of disease in primate
ecology, behavior, and evolution; and to examine how
anthropogenic effects alter the zoonotic potential of
Howler Monkeys as Sentinels for Conservation and Health / 81
various pathogenic organisms. Considering the evolutionary and ecological links between primates and
their pathogens, observing changes in patterns of
infection by naturally occurring pathogens in sentinels like black and gold howlers has the capacity to
alert us to potentially imminent threats to primate
conservation and human health.
ACKNOWLEDGMENTS
The study complies with the current laws of the
countries in which it was conducted (IACUC protocol
06207). We thank our field assistants and collaborators who helped collect samples: Silvana Peker,
Romina Pave, Amparo Perez-Rueda, Ramon Martinez,
and Miguel Blanco. Silvana Peker also provided a
vehicle (R12) to visit different field sites.
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