American Journal of Primatology 71:1–10 (2010)

RESEARCH ARTICLE
Gastrointestinal Parasites of Howler Monkeys (Alouatta palliata) Inhabiting the
Fragmented Landscape of the Santa Marta Mountain Range, Veracruz, Mexico
CAROLINA VALDESPINO1, GUILLERMO RICO-HERNÁNDEZ2, AND SALVADOR MANDUJANO1
1
Biologı´a y Conservación de Vertebrados, Instituto de Ecologı´a, Xalapa, Veracruz, Mexico
2
Conzooltores Ltda., Bogotá, Colombia

In recent years populations of howler monkeys (Alouatta palliata) in southeastern Mexico have
decreased substantially due to the transformation and loss of natural habitats. This is especially evident
in the Santa Marta mountain range, Veracruz, Mexico where several studies have evaluated the impact
of fragmentation on howler monkey populations in order to propose management programs for their
conservation. The conditions generated by fragmentation likely change the rates of parasitic infection
and could decrease howler survival. In this study, gastrointestinal parasite species richness, prevalence,
and egg density of infection were determined in howler groups inhabiting five forest fragments at the
Santa Marta mountain range. Two hundred and seventy-eight fresh fecal samples were collected
between October 2002 and April 2003. Three parasite species were found during the dry and the wet
season in all forest fragments sampled: one unidentified species of Eimeriidae; Trypanoxyuris minutus
(Oxyuridae); and Controrchis biliophilus (Dicrocoeliidae). Both the prevalence of T. minutus and
infection density for all parasites differed between seasons and fragments (the largest fragment
consistently differed from other fragments). Host density, distance to the nearest town, fragment size,
fragment shape, and total basal area of food trees explained parasite prevalence, but each species had a
different pattern. Although parasite richness was lower, prevalence and density were higher than
values reported for howlers in conserved forests. These results suggest that the establishment of
biological corridors and animal translocation programs must take into account the parasite ecology of
each fragment to avoid higher infection rates and preclude potential consequent mortality. Am. J.
Primatol. 71:1–10, 2010. r 2010 Wiley-Liss, Inc.

Key words: Mexican mantled howler monkey; prevalence; forest fragment; Trypanoxyuris
minutus; Controrchis biliophilus; coccidia; total basal area; food tree species

INTRODUCTION health and physiological stress response of fragment

Habitat fragmentation is considered the main
reason for biodiversity decline [Turner et al., 1996;
Wilcox & Murphy, 1985], and primate species are of
special concern because massive changes have
occurred in the tropical forests that they inhabit
[Chapman & Peres, 2001; Cowlishaw & Dunbar,
2000]. As a result, in recent years many studies have
focused on different aspects of primate biology and
survivorship with the purpose of understanding the
ecological challenges they face in these transformed
environments [e.g. Arroyo-Rodrı́guez & Mandujano,
2009]. The attributes of forest fragments (e.g. shape
and size, spatial arrangement, plant species diver-
sity, changes in predation risk) affect dietary
strategies [Cristóbal-Azkarate & Arroyo-Rodrı́guez,
2007; Saunders et al., 1991]; carrying capacity
[Arroyo-Rodrı́guez & Mandujano, 2006; Arroyo-
Rodrı́guez et al., 2007; Worman & Chapman, 2006];
opportunities for dispersal [Cristóbal-Azkarate et al.,
2005; Wahungu et al., 2005]; group size [Dias &
Rodrı́guez-Luna, 2006; Zunino et al., 2007], and the
inhabitants [Martı́nez-Mota et al., 2007].
A common recommendation of conservation-
oriented studies is to increase forest fragment
size or to connect them with biological corridors
by means of reforestation [Escobedo-Morales &
Mandujano, 2007; Rodrı́guez-Toledo et al., 2003].
The objectives of forest expansion are to facilitate
long distance dispersal and to increase gene flow
between isolated populations [Fahrig & Merriam,
1994; Juan-Solano et al., 2000; Mandujano et al.,
Contract grant sponsors: The American Society of Primatolo-
gists; The Dirección General de Relaciones Internacionales-SEP.
Correspondence to: Carolina Valdespino, Biologı́a y Conserva-
ción de Vertebrados, Instituto de Ecologı́a, A.C. km. 2.5 Antigua
Carretera a Coatepec No. 351, Congregación El Haya, Xalapa,
Veracruz, Mexico. E-mail: carolina.valdespino@inecol.edu.mx
Received 20 March 2009; revised 7 January 2010; revision
accepted 8 January 2010
DOI 10.1002/ajp.20808
Published online in Wiley InterScience (www.interscience.
wiley.com).

r 2010 Wiley-Liss, Inc.

2 / Valdespino et al.
2004, 2005; Palacios-Silva & Mandujano, 2007].
Owing to recent pro-active political conservation
and restoration strategies, in some tropical regions
(e.g. Veracruz state, Mexico) these management
policies are underway [Robles-Martı́nez, 2009]. How-
ever, little is known concerning the potential health
risks faced by isolated primate populations when
individuals from different forest fragments come into
contact [Chapman et al., 2005].
Endoparasites are a natural component of
ecological systems; however, habitat transformation
may alter host–parasite dynamics [Altizer et al.,
2003; Nunn et al., 2003], parasite virulence or
parasite host range [Daszak et al., 2000], resulting
in changes in host susceptibility and infection risk.
For example, it has been suggested that dietary
stress (that probably occurs in forests that have
been reduced in size) may exacerbate the clinical
consequences of parasitic infection through immuno-
suppression [Holmes, 1995; Milton, 1996]. Endo-
parasites can affect an animal’s health by their
pathological effects or by reducing the condition of
the host [Chapman et al., 2006b]. This could result in
elevated morbidity and mortality, and ultimately,
population decline.
Risks can differ depending on whether the
parasite life cycle is direct and infection results from
contact with infected material (feces) from co-
specifics, contaminated food or water. Infection can
also be indirect, when there is need of an inter-
mediate host (usually an invertebrate) before the
development of the adult form in the definite host
[Sloss et al., 1994]. It has been suggested that in
disturbed habitats direct cycle parasites may benefit
from increased host crowding and reduced competi-
tion with parasites that have an indirect life cycle
[Trejo-Macı́as et al., 2007], and under these circum-
stances the intermediate hosts of indirect life cycle
parasites may be also disappearing.
An arboreal lifestyle may protect primates from
exposure to infection from parasites that have a
direct life cycle by limiting contact with the ground,
which may be contaminated with eggs or cysts
[Stuart et al., 1990]. However, during the process
of fragmentation, as available habitat decreases,
hosts are crowded into the remaining fragments
with the consequence that the spread of density-
dependent diseases and parasitic infections may be
facilitated [Nunn et al., 2003]. The edges created by
disturbance on forest landscapes may cause changes
in the ecology of the host or parasite, or both. For
example, the proportion of individuals with multiple
infections, associated with a greater potential for
morbidity and mortality [Chapman et al., 2005], is
greater in the edge of the forest than in its interior
[Chapman et al., 2006a]. With increasing fragmenta-
tion arboreal primates may be forced to descend to
the ground to cross gaps in the forest canopy, reach
sources of water, or move between forest fragments
Am. J. Primatol.
[see Bicca-Marques & Calegaro-Marques, 1995], resul-
ting in an increased probability of contact with
domestic animals or infected human material, thus
increasing parasite transmission compared with popu-
lations that inhabit undisturbed habitats [Chapman
et al., 2005; May, 1988; Miropé-Santa Cruz et al.,
2001]. As a consequence, biological corridors may
facilitate the movement of not only the individuals
between forest fragments, but also that of native and
exotic parasite species [Hess, 1994, 1996], spreading
parasitic infections to healthy isolated groups.
Mantled howler monkeys (Alouatta palliata), one
of the three native primate species of Mexico, are
classified as vulnerable [IUCN, 2002]. Several studies
have identified the presence of endoparasites in howler
populations [De Thoisy et al., 2001; Gilbert, 1994;
Hugghins, 1969; Kopper-Müller et al., 2000; Miropé-
Santa Cruz et al., 2001; Stoner, 1996; Stoner &
González-Di Pierro, 2005; Stuart et al., 1990, 1998].
In this study we use noninvasive methodologies (1) to
compare gastrointestinal parasite richness, prevalence,
and egg density [sensu Bush et al., 1997, number of
parasites in a measured sampling unit taken from a
host] for A. palliata living in different forest fragments;
(2) to analyze seasonal changes in the three variables;
(3) to calculate the prevalence of multiple infections;
and (4) to evaluate the role of host density, forest
fragment shape, forest fragment size, availability of
food tree species, and distance to towns on parasite
prevalence. Our objective is to provide a database that
can be used to make informed recommendations for
conservation programs designed to construct forest
corridors between fragmented primate populations.
METHODS
Study Site
The study was conducted between October 2002
and April 2003, and included data collected during
both the wet (October–December) and the dry
(February–April) seasons. Five rainforest fragments
(Fig. 1), located within a total area of 3987 ha in the
Santa Marta mountain range, Veracruz (181180 N
and 941500 W), were selected for study. These frag-
ments have an arboreal stratum 410 m and have
been isolated for 30–40 years. The general vegetation
and site characteristics of the Santa Marta mountain
range have been reported elsewhere [Arroyo-
Rodrı́guez et al., 2008; Rodrı́guez-Toledo et al.,
2003]. The human population in the area surround-
ing the patches is about 1,200, and all fragments are
bordered by pastures [Robles-Martı́nez, 2009].
Previous research indicated that these frag-
ments rank as high-priority targets for conservation
because they offer adequate patch size for howlers,
because of the number of primates living in them,
and the possibility of creating biological corridors to
connect them [Rodrı́guez-Toledo et al., 2003]. Frag-
ment size and howler density are reported in Table I.
 Parasites of Howlers in Forest Fragments / 3

Fig. 1. Map showing the forest fragments studied on the Santa Marta mountain range landscape in Veracruz. Areas with diagonal lines
are towns (Magallanes, population 243, is given as an example). Lined patches are not occupied by howler monkeys; black patches are
occupied by howler monkeys; the fragments studied are in black and labelled A–E (these have conservation and restoration priority).
Solid lines are roads and dotted lines are rivers.

TABLE I. Characteristics of the Forest Fragments Sampled on the Santa Marta Mountain Range in Veracruz,
Mexico. The Number of Hosts and Feces Collected are Shown as well

TBA-food Distance to Density No. feces

Fragment Size (ha) Shape trees (m2) nearest town (m) No. howlers (ind/ha) collected

A 6.57 2.22 1.16453143 611 5 0.76 30

B 9.65 1.48 2.99099955 2,000 8 0.83 48
C 11.86 1.47 0.49628248 0 13 1.10 85
D 30.06 4.32 2.83891725 560 11 1.20 85
E 57.18 2.88 3.49037258 330 6 0.11 30

Am. J. Primatol.
4 / Valdespino et al.
Attributes of the Forest Fragments
The landscape characteristics of the Santa
Marta mountain range forest fragments have been
reported elsewhere [Arroyo-Rodrı́guez et al., 2007,
2008]. Briefly, the landscape has been digitized
with ArcView 3.2 (Environmental System Research
Institute, Inc., Redlands, CA) using aerial photo-
graphs (1:20,000), orthophotos, digital data, and field
information [Arroyo-Rodrı́guez et al., 2005]. Size,
distance to the nearest village, and shape for all
patches (Table I) were calculated using the Patch
Analyst 2.2 extension. The shape index of each patch
is calculated as SI 5 P/OAp; where P is the perimeter
and A is the area, in meters [Forman & Godron,
1986]. Index values vary from 1, for a circular shape,
to 5 for a highly irregular shape. A rounded shape is
thought to cause fewer edge-related effects for
populations inhabiting these areas.
Information on food tree species in each frag-
ment was collected between January 2004 and May
2005, following Gentry’s [1982] protocol on ten
transects (50  2 m) randomly placed in each frag-
ment as previously reported [Arroyo-Rodrı́guez
et al., 2007]. All tree, shrub, and liana species with
diameter at breast height (dbh) Z10 cm were
recorded. Plant species that constitute 480% of
total howler feeding time at Los Tuxtlas [Fig. 1;
Cristóbal-Azkarate & Arroyo-Rodrı́guez, 2007] were
considered tree food species and their total basal area
(TBA) was calculated for each fragment (Table I).
Fecal Sampling and Processing
Fresh howler fecal samples were collected once
per month, immediately upon defecation. Collection
took place during the same week and fragments were
visited in a random order. As we could not individually
recognize each of the animals, samples from each
group were collected early in the morning of a single
day, moving along the group so as not to repeatedly
sample the same individual. This methodology has
been used previously by other authors studying
parasite loads in primates, and is designed to
calculate an index of parasite prevalence [Chapman
et al., 2005, 2006a; Gillespie & Chapman, 2008]. As
the number of howlers in each fragment differed, a
different number of samples were collected in each
(Table I). Given that the howlers were unable to
travel between forest fragments, the parasite infor-
mation presented in this study is fragment specific.
Feces were preserved in vials with 5% buffered
formalin and transported to the Instituto de Biologı́a,
UNAM where endoparasite eggs and oocytes were
separated using sodium nitrate flotation and ether
sedimentation methods [Sloss et al., 1994]. The color,
shape, and size of the eggs and oocytes were used to
identify the parasite species, and egg density was
obtained using a McMaster counting chamber.
Densities are reported as no. of eggs/g of feces.
Am. J. Primatol.
Data Analysis
Many factors can affect the number of eggs
produced by parasites and contained in the host fecal
material [Gillespie, 2006]. Also, Stuart et al. [1990]
found that although 100% of A. palliata (N 5 155) at
their study site in Costa Rica was infected with
T. minutus (as evidenced by peri-anal examination),
eggs were present in only 22% of the fecal samples
collected, therefore we used samples collected over
three consecutive months to describe each season
and reduce measurement error.
For each parasite the square root arcsine trans-
formed index of prevalence and log-transformed
egg parasite density were compared by fragment
and by season with two-way analyses of variance
(ANOVAs). The prevalence of multiple infections
was analyzed with a two-way ANOVA as well. In
order to have an equal number of replicates per cell
for optimum power [Zar, 1974], a random selection of
the samples analyzed in the lab was used in the
statistical analyses of egg density.
Using generalized linear models [GLM; Crawley,
2002] we selected the combination of two predictors
that best explained the square root arcsine trans-
formed index of prevalence for each parasite. We
could only use two predictors because we only had
ten data on prevalence (two per patch). The
predictors used were monkey density (to evaluate
density dependence); food resource availability (mea-
sured as TBA of howler food species); distance to the
nearest town; and size and shape of the forest
fragment (as a measure of habitat quality). We used
a separate slope model with a normal distribution
and a log-link function, and tested for collinearity
between predictor variables [Chatterjee et al., 2000].
Sampling season was included as the categorical
variable in the model.
All analyses were run with STATISTICA 7.1
(StatSoft, Inc 1984–2006).
Ethics
This research adheres to the American Society of
Primatologists (ASP) Principles for the Ethical
Treatment of Nonhuman Primates. Research proto-
cols reported in this manuscript were approved by
the National Wildlife Commission of SEMARNAT
(Mexican Secretary for the Environment and Natural
Resources), and adhered to the legal requirements of
Mexico.
RESULTS
A total of 278 fecal samples were collected
(Table I). Species richness for all forest frag-
ments was the same, and was composed of three
species: one unidentified Eimeriidae protozoan
(probably Isospora arctopitheci, Michael Stuart,
 Parasites of Howlers in Forest Fragments / 5

personal communication); the Oxyuridae nematode,
Trypanoxyuris minutus; and the Dicrocoeliidae pla-
tyhelminth, Controrchis biliophilus.
Only the prevalence of T. minutus differed
between fragments (F 5 7.5501, df 5 4, P 5 0.04;
Fig. 2) and seasons (23.23% in the dry and 51.13%
in the wet season; F 5 18.0135, df 5 1, P 5 0.01;
Fig. 3). A Tukey post hoc test indicated that the
difference between fragments is due to differences in
parasite prevalence in the howlers of fragment A (the
smallest fragment, 52.87%) and those of fragment E
(the largest fragment, 9.09%).
There were no significant differences in the pre-
valence of multiple infections per season or fragment,

100 80

80
Eimeriidae Prevalence

60

Eimeriidae Prevalence
60

40
40

20 20

0
0
A A B C D E
A Wet Dry
80
70

60
60
T. minutus Prevalence

T. minutus Prevalence

50

40
40
30

20 20

10

0
0
B A B C D E
B Wet Dry
100
60

80 50
C. biliophilus Prevalence

C. biliophilus Prevalence

40
60

30
40
20

20
10

0 0
A B C D E Wet Dry
C FOREST FRAGMENTS C FOREST FRAGMENTS
Fig. 2. Indices of prevalence (mean7standard error; calculated Fig. 3. Indices of prevalence (mean7standard error; calculated
as detailed in Methods) found for the howler monkeys of the as detailed in Methods) found for the howler monkeys of the
fragmented landscape shown per forest fragment. Eimeriidae sp. fragmented landscape shown per season. Eimeriidae sp. (A);
(A); Trypanoxyuris minutus (B) and Controrchis biliophilus (C). Trypanoxyuris minutus (B) and Controrchis biliophilus (C).

Am. J. Primatol.
6 / Valdespino et al.

but it was higher in the wet months (27.22%) than that in fragment E (the largest), the density of
during the dry ones (10.36%). T. minutus (lowest) and C. biliophilus (highest) differed
The density of eggs in feces for all parasite from that of fragments A and B in both cases. And also
species (Table II) differed between fragments from fragment C, only in the case of C. biliophilus.
(Eimeriidae sp., F 5 7.83, df 5 4, P 5 0.00001; Meanwhile values were intermediate for the Eimeriidae
T. minutus, F 5 4.40, df 5 4, P 5 0.0025; C. biliophilus, sp. in that largest fragment, compared with the other
F 5 5.52, df 5 4, P 5 0.0004) and seasons (Eimeriidae fragments (higher: A and B, lower: C and D). The
sp., F 5 29.83, df 5 1, P 5 0.0000003; T. minutus, density of Eimeriidae sp. and T. minutus eggs were
F 5 20.77, df 5 1, P 5 0.00001; C. biliophilus, F 5 6.05, higher during the wet season while C. biliophilus
df 5 1, P 5 0.015). The Tukey post hoc test showed density was higher during the dry season.
The generalized linear models for the prevalence
of each parasite are listed in Table III. Eimeriidae sp.
TABLE II. Egg Density of Parasite Species (egg/gr, prevalence was best explained by host density and
mean7standard error) Recorded from Feces of distance to the nearest town although only the
Alouatta palliata Inhabiting Forest Fragments at second predictor was significant during the dry
Sierra de Santa Marta Mountain Range. Egg Count season. The model for T. minutus prevalence
Done with a McMaster Counting Chamber included fragment shape and size as the best
Eimeriidae sp. T. minutus C. biliophilus
predictors during both seasons. C. biliophilus pre-
valence was associated with distance to the nearest
Fragment town and the TBA of top food species, but during the
Fragment A 111.36721.30 109.09715.30 56.8273.74 wet season only the latter predictor was significant.
Fragment B 113.64720.06 88.64710.88 54.5573.14
Fragment C 52.2772.27 79.5576.29 56.8273.74
Fragment D 54.5574.55 79.5578.49 77.27710.77 DISCUSSION
Fragment E 79.5578.49 54.5573.14 81.8276.19 Although the endoparasite species richness of
Season howler monkeys (A. palliata) did not vary across the
Wet 108.18711.84 100.9177.77 59.0972.90
five isolated forest patches in this fragmented land-
Dry 56.3672.59 63.6473.27 71.8274.94
scape, parasite prevalence and egg density were

TABLE III. Results of the Generalized Linear Models for the Three Parasite Species Found in Alouatta palliata
in the Santa Marta Mountain Range in Veracruz, Mexico

Effect Estimate Standard error w2 P

Eimeriidae sp.
Intercept 2.64207 0.399637 43.70751 0.000000
Wet seasonHowler density 1.10949 0.310474 12.77009 0.000352
Dry seasonHowler density 0.55619 0.526119 1.11759 0.290439
Wet seasonD. nearest town 0.00047 0.000141 10.95668 0.000933
Dry seasonD. nearest town 0.00045 0.000218 4.26707 0.038858
Wet season 0.93744 0.435178 4.64038 0.031228
Dry season 0.00000
Scale 0.02601 0.005815 20.00000 0.000008
T. minutus
Intercept 2.58447 0.159395 262.9012 0.000000
Wet seasonFragment size 0.01211 0.002677 20.4573 0.000006
Dry seasonFragment size 0.05286 0.010949 23.3092 0.000001
Wet seasonFragment shape 0.09443 0.039116 5.8281 0.015772
Dry seasonFragment shape 0.41205 0.108015 14.5520 0.000136
Wet season 0.63094 0.178164 12.5412 0.000398
Dry season 0.00000
Scale 0.01020 0.002281 20.0000 0.000008
C. biliophilus
Intercept 2.77268 0.173923 254.1463 0.000000
Wet seasonD. nearest town 0.00022 0.000132 2.8636 0.090602
Dry seasonD. nearest town 0.00120 0.000260 21.2703 0.000004
Wet seasonTBA food trees 0.21077 0.073862 8.1429 0.004323
Dry seasonTBA food trees 0.42954 0.056399 58.0057 0.000000
Wet season 0.18718 0.270261 0.4797 0.488564
Dry season 0.00000
Scale 0.01259 0.002814 20.0000 0.000008

Am. J. Primatol.

found to differ. Overall, egg density varied seasonally
and the availability of food, host density, fragment
size and shape as well as the distance to the nearest
town seemed to be associated with parasite preva-
lence, each parasite following a different pattern.
We found that the nematode (T. minutus) and
the trematode (C. biliophilus), previously reported
for A. palliata in southern Mexico [Trejo-Macı́as
et al., 2007] and Costa Rica [Chinchilla et al., 2005;
Stuart et al., 1990], were also present in our study
population. Trypanoxyuris also has been found in
several species of Alouatta in Brazil, Colombia, and
Surinam [Stuart et al., 1990, 1993, 1998]. We also
found an Eimeriidae coccidian which may correspond
to I. arctopitheci previously reported for A. palliata
in Costa Rica [Stuart et al., 1990], A. pigra in
Chiapas, Mexico [Stoner, 1996] and A. villosa in
Panama [Hendricks, 1977].
T. minutus and the Eimeriidae sp. have a direct
life cycle. Adult T. minutus live in the colon [Müller,
2007] and the Eimeriidae sp. develop within the endo-
thelial cells of the gastrointestinal tract [Duszynski
et al., 1999]. Both produce oocysts that leave the host
via the feces and immediately infect the next host to
ingest them from contaminated food or water. In
contrast, C. biliophilus has a very complex cycle that
requires two intermediate hosts. The first is believed
to be a snail and the second is hypothesized to be
ants [Vitazkova & Wade, 2006].
The number of parasite species found is consis-
tent with previous reports for other howlers studied
in the state of Veracruz. [Canales-Espinosa, 1992;
Lamothe-Argumedo et al., 1997; Villanueva-Jiménez,
1988]. However, the species of parasites differed. In
contrast, Trejo-Macı́as et al. [2007] report up to six
parasite species (three trematodes, two nematodes,
and one species of Coccidea) in A. palliata, in a large-
scale survey of protected continuous and fragmented
forests in Veracruz, Chiapas and Campeche, Mexico.
These authors suggest that the parasite richness
reported for primate groups from protected and
continuous forests more closely resembles natural
parasite–host ecological relationships than those
found in primates inhabiting more fragmented land-
scapes. This supports the idea that human pressures
that reduce the size of the host population may lead to
a reduction in parasite species numbers [Altizer et al.,
2007]. In particular, disturbed habitats are believed to
benefit parasites with direct cycles by increasing host
crowding and reducing competition with indirect life
cycle parasites [Trejo-Macı́as et al., 2007].
In this study of five forest fragments we found a
higher prevalence of parasites with both a direct
(T. minutus) and an indirect (C. biliophilus) life cycle
than those reported for howlers inhabiting protected
and less isolated forests [Chinchilla Carmona et al.,
2005; Trejo-Macı́as et al., 2007]. Parasites do not
usually cause the death of the host; however, the
death of a male A. guariba that had a hyper-infection
Parasites of Howlers in Forest Fragments / 7
of T. minutus [Amato et al., 2002] is a warning that
when the physical condition of the host is poor due to
food shortage [Chapman et al., 2006b] or physiologi-
cal stress [Martı́nez-Mota et al., 2007], parasite
infection may result in death.
We also recorded something that has not been
reported for A. palliata living in continuous, protected
forests: a higher prevalence (29%) of coccidian para-
sites at our study site; even higher than that reported
in other fragmented forests [9%, Trejo-Macı́as et al.,
2007]. This is of particular concern because coccidiosis
is a major health hazard for domestic and wild animals
under crowded conditions [Duszynski et al., 1999;
Foreyt, 2001] and in high humidity [Moreno-Dı́az &
Ibarra-Velarde, 2002]. Where there has been defor-
estation, domestic and wild animals come into contact
more frequently because of forest edge effects
[Chapman et al., 2006b]. I. arctopitheci is recognized
as a unique coccidian due to the unusually wide range
of hosts that it can infect. It has been reported in
several primate species [the tamarin, Saguinus geof-
froyi, the capuchin, Cebus capucinus, the night
monkey, Aotus trivirgatus, the spider monkey, Ateles
fuscipes, the howler, A. pigra, and the squirrel monkey,
Saimiri sciureus; Duszynski et al., 1999], as well as in
the domestic cat and dog, several wild carnivores, the
opossum and humans [Hendricks, 1977]. Cross-infec-
tion is probably more frequent in the forest fragments
where humans and domestic animals (dogs, cattle,
sheep) wander around, increasing the number of hosts
(in addition to the wild ones, i.e. howlers, opossums,
coatis, and kinkajous). This is the case in the Santa
Marta mountain range. We do not have data on the
prevalence of coccidiosis in domestic animals for the
Santa Marta mountain range area; however, it is
known to be a significant problem for sheep, cattle, and
poultry farmers in the state of Veracruz [Moreno-Dı́az
& Ibarra-Velarde, 2002].
The prevalence of the nematode T. minutus was
found to differ across forest fragments and between
seasons. Prevalence was lowest in the largest frag-
ment (in contrast to the smallest and least circular
ones) and during the dry season. Troop membership
has previously been described as the principal factor
for predicting infection with T. minutus in A. pigra
[Vitazkova & Wade, 2007]. Some authors also state
that the infectious form in nematodes only develops
under special conditions [Chinchilla Carmona et al.,
2005], and high humidity may be one of them.
In contrast, there was no relationship between
the prevalence of the other two parasites or multiple
infections and the fragment characteristics or season
of the year. Some authors have emphasized the
importance of multiple infection indices as a measure
of environmental health [Chapman et al., 2006a,b;
Trejo-Macı́as et al., 2007]. Prevalence and egg
density of multiple infections are higher for red
colobus (Piliocolobus tephrosceles) inhabiting frag-
mented forests than those inhabiting nonfragmented
Am. J. Primatol.
8 / Valdespino et al.
ones [Gillespie & Chapman, 2008]. In addition,
multiple infections are more prevalent in colobus
living at the forest edge than in those living in the
interior of the fragment [Chapman et al., 2006a]. In
our study, the prevalence of multiple infection
ranged from 0 to 45% and contrasts with the absence
of multiple infection reported by Trejo-Macı́as et al.
[2007] in their broad-scale survey of parasites in
A. palliata from fragmented and conserved forests.
We found that fragment traits explain parasite
prevalence but the explanatory trait differed for each
parasite. This is most likely associated with the
parasite’s cycle and the conditions needed for trans-
mission. For example: the availability of food tree
species was directly associated with the prevalence of
C. biliophilus. This might result from the greater
amount of food trees that are found in forests of better
quality which, in turn, may allow the presence of the
intermediate hosts (snails and ants) needed for the
development of this parasite. This hypothesis is also
supported by the significant association with the
distance to the nearest town, suggesting that less
disturbance is associated with higher prevalence.
During the wet season, however, prevalence is only
associated with the availability of top food species.
For T. minutus, larger fragments and irregular
fragment shapes were associated with lower pre-
valence. This may be due to the fact that, in our
study, larger fragments corresponded to those with
the more irregular shapes. This means that a large
size in a fragment minimizes edge-related effects
caused by irregular forest peripheries.
Harder to explain is the model found for the
prevalence of Eimeriidae sp., given that an inverse
relationship was found with host density and a direct
one with distance to the nearest town. Coccidean
parasites are closely associated with crowded condi-
tions [Duszynski et al., 1999; Foreyt, 2001] but this
does not seem to apply in this study. However, the
higher prevalence in fragments farther away from
towns may indicate that their presence requires less-
disturbed localities where other wild, free-ranging
hosts may be present as well [Hendricks, 1977]. As
mentioned above, the forest fragments studied (and
the larger ones probably more) are inhabited by
several species of medium-sized animals which are
hosts for this parasite as well.
Finally, the characteristics of the fragments
studied do not lie along a gradient. That is, the
fragments that are located farther from towns are
not the largest, nor are they the least crowded. This
reduces the chances of detecting clear relationships.
The aim of our study was to reveal the role of
seasonality and this made it necessary to use a small
number of fragments. A broader survey during
different seasons may further clarify the trends
observed here. However, our findings in this study
of A. palliata and its parasites in the fragmented
landscape of the Santa Marta mountain range do
Am. J. Primatol.
seem to support the idea that habitat transformation
changes host–parasite dynamics [Altizer et al., 2003;
Nunn et al., 2003], parasite virulence and parasite
host range [Daszak et al., 2000].
Seasonal variation in parasite infection needs to
be evaluated for any population to be included in
conservation management practices. Egg density for
all parasites varied with season and fragment.
Density for both of the parasites with a direct life
cycle, the Eimeriidae sp. and T. minutus, was higher
during the wet season, whereas density for
C. biliophilus was higher during the dry season. High
values of C. biliophilus during the dry season have
been previously reported in A. pigra, but as elevated
prevalence [Vitazkova & Wade, 2007]. The largest
forest fragment was characterized by an intermediate
density of the Eimeriidae sp., a higher density of
C. biliophilus, and lower egg density for T. minutus.
In conclusion, the conservation and management
practices of threatened and endangered primates
must take into account the effects of environmental,
demographic, behavioral, and human trends when
assessing infection rates [Stuart & Strier, 1995]. In
the Santa Marta mountain range we found that para-
site richness does not differ among howler groups
living in different forest fragments. This suggests
that the proposal of setting forest corridors to
promote primate dispersal and gene flow [Escobedo-
Morales & Mandujano, 2007; Rodrı́guez-Toledo et al.,
2003] could be innocuous. However, lower parasite
species richness than that of howlers in protected
forests, as well as differences in the prevalence and
egg density of the parasites recorded among the
fragments warn us to be cautious when designing
these corridors. For example, increased connectivity
between fragments could reduce global prevalence of
T. minutus, as this species was least prevalent in the
largest fragments. However, it may as well result in
the increased prevalence of Eimeriidae sp. because
the other wild hosts will also be able to move
along the corridors. Human induced migration and
contact between two different colobus species (the
red colobus, P. tephrosceles and the black-and-white
colobus, Colobus guereza) has already resulted in the
increased prevalence of parasites that seem to have
led to a decline in the black-and-white colobus
population [Chapman et al., 2005]. Therefore, if
effective conservation policies are to be put into
practice epidemiological information should be taken
into account. For example, an initial increase in the
area of each fragment (by reforesting the perimeter)
could even out parasite infection in all of the
fragments to be connected. Also, as this and other
studies [Chapman et al., 2006b] have demonstrated,
food availability is an important factor in determin-
ing parasite prevalence. Reforestation with tree
species used by the howlers as food could accelerate
evenness in parasite infection before the corridor
reforestation solution is put into practice.

ACKNOWLEDGMENTS
We thank Ruben Mateo and his family for
assistance in the field and for storing the samples.
Guillermo Salgado and David Osorio gave advice and
assistance in the laboratory. Dr. Michael Stuart
corroborated our identification of parasites and gave
a taxonomic position for the Coccidean parasite.
Dr. Vinicio Sosa helped with the statistical analysis of
the data and Rodolfo Martı́nez-Mota revised an earlier
version of this manuscript. Bianca Delfosse improved
the English. This research complies with protocols
approved by the National Wildlife Commission of
SEMARNAT (Mexican Secretary for the Environment
and Natural Resources), and the legal requirements of
Mexico.
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