Gastrointestinal parasites of howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Sierra Santa Marta mountain range, Mexico

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American Journal of Primatology 71:110 (2010)

RESEARCH ARTICLE

Gastrointestinal Parasites of Howler Monkeys (Alouatta palliata) Inhabiting theFragmented Landscape of the Santa Marta Mountain Range, Veracruz, Mexico

CAROLINA VALDESPINO1, GUILLERMO RICO-HERNANDEZ2, AND SALVADOR MANDUJANO11Biologa y Conservacion de Vertebrados, Instituto de Ecologa, Xalapa, Veracruz, Mexico2Conzooltores Ltda., Bogota, Colombia

In recent years populations of howler monkeys (Alouatta palliata) in southeastern Mexico havedecreased substantially due to the transformation and loss of natural habitats. This is especially evidentin the Santa Marta mountain range, Veracruz, Mexico where several studies have evaluated the impactof fragmentation on howler monkey populations in order to propose management programs for theirconservation. The conditions generated by fragmentation likely change the rates of parasitic infectionand 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 theSanta Marta mountain range. Two hundred and seventy-eight fresh fecal samples were collectedbetween October 2002 and April 2003. Three parasite species were found during the dry and the wetseason in all forest fragments sampled: one unidentified species of Eimeriidae; Trypanoxyuris minutus(Oxyuridae); and Controrchis biliophilus (Dicrocoeliidae). Both the prevalence of T. minutus andinfection density for all parasites differed between seasons and fragments (the largest fragmentconsistently 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 adifferent pattern. Although parasite richness was lower, prevalence and density were higher thanvalues reported for howlers in conserved forests. These results suggest that the establishment ofbiological corridors and animal translocation programs must take into account the parasite ecology ofeach fragment to avoid higher infection rates and preclude potential consequent mortality. Am. J.Primatol. 71:110, 2010. r 2010 Wiley-Liss, Inc.

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

INTRODUCTION

Habitat fragmentation is considered the mainreason for biodiversity decline [Turner et al., 1996;

Wilcox & Murphy, 1985], and primate species are ofspecial concern because massive changes haveoccurred in the tropical forests that they inhabit[Chapman & Peres, 2001; Cowlishaw & Dunbar,2000]. As a result, in recent years many studies havefocused on different aspects of primate biology and

survivorship with the purpose of understanding theecological challenges they face in these transformedenvironments [e.g. Arroyo-Rodrguez & Mandujano,2009]. The attributes of forest fragments (e.g. shapeand size, spatial arrangement, plant species diver-sity, changes in predation risk) affect dietarystrategies [Cristobal-Azkarate & Arroyo-Rodrguez,2007; Saunders et al., 1991]; carrying capacity[Arroyo-Rodrguez & Mandujano, 2006; Arroyo-Rodrguez et al., 2007; Worman & Chapman, 2006];opportunities for dispersal [Cristobal-Azkarate et al.,2005; Wahungu et al., 2005]; group size [Dias &Rodrguez-Luna, 2006; Zunino et al., 2007], and the

health and physiological stress response of fragmentinhabitants [Martnez-Mota et al., 2007].

A common recommendation of conservation-oriented studies is to increase forest fragmentsize or to connect them with biological corridorsby means of reforestation [Escobedo-Morales &Mandujano, 2007; Rodrguez-Toledo et al., 2003].The objectives of forest expansion are to facilitatelong distance dispersal and to increase gene flow

between isolated populations [Fahrig & Merriam,1994; Juan-Solano et al., 2000; Mandujano et al.,

Published online in Wiley InterScience (www.interscience.wiley.com).

DOI 10.1002/ajp.20808

Received 20 March 2009; revised 7 January 2010; revisionaccepted 8 January 2010

Contract grant sponsors: The American Society of Primatolo-gists; The Direccion General de Relaciones Internacionales-SEP.

Correspondence to: Carolina Valdespino, Biologa y Conserva-cion de Vertebrados, Instituto de Ecologa, A.C. km. 2.5 AntiguaCarretera a Coatepec No. 351, Congregacion El Haya, Xalapa,

Veracruz, Mexico. E-mail: [email protected]

r 2010 Wiley-Liss, Inc.


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2004, 2005; Palacios-Silva & Mandujano, 2007].Owing to recent pro-active political conservationand restoration strategies, in some tropical regions(e.g. Veracruz state, Mexico) these managementpolicies are underway [Robles-Martnez, 2009]. How-

ever, little is known concerning the potential healthrisks faced by isolated primate populations whenindividuals from different forest fragments come intocontact [Chapman et al., 2005].

Endoparasites are a natural component ofecological systems; however, habitat transformationmay alter hostparasite dynamics [Altizer et al.,2003; Nunn et al., 2003], parasite virulence orparasite host range [Daszak et al., 2000], resultingin changes in host susceptibility and infection risk.For example, it has been suggested that dietarystress (that probably occurs in forests that havebeen reduced in size) may exacerbate the clinicalconsequences of parasitic infection through immuno-

suppression [Holmes, 1995; Milton, 1996]. Endo-parasites can affect an animals health by theirpathological effects or by reducing the condition ofthe host [Chapman et al., 2006b]. This could result inelevated morbidity and mortality, and ultimately,population decline.

Risks can differ depending on whether theparasite life cycle is direct and infection results fromcontact with infected material (feces) from co-specifics, contaminated food or water. Infection canalso be indirect, when there is need of an inter-mediate host (usually an invertebrate) before thedevelopment of the adult form in the definite host

[Sloss et al., 1994]. It has been suggested that indisturbed habitats direct cycle parasites may benefitfrom increased host crowding and reduced competi-tion with parasites that have an indirect life cycle[Trejo-Macas et al., 2007], and under these circum-stances the intermediate hosts of indirect life cycleparasites may be also disappearing.

An arboreal lifestyle may protect primates fromexposure to infection from parasites that have adirect life cycle by limiting contact with the ground,which may be contaminated with eggs or cysts[Stuart et al., 1990]. However, during the processof 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 befacilitated [Nunn et al., 2003]. The edges created bydisturbance on forest landscapes may cause changesin the ecology of the host or parasite, or both. Forexample, the proportion of individuals with multipleinfections, associated with a greater potential formorbidity and mortality [Chapman et al., 2005], isgreater 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 tothe ground to cross gaps in the forest canopy, reachsources of water, or move between forest fragments

[see Bicca-Marques & Calegaro-Marques, 1995], resul-ting in an increased probability of contact withdomestic animals or infected human material, thusincreasing parasite transmission compared with popu-lations that inhabit undisturbed habitats [Chapman

et al., 2005; May, 1988; Mirope-Santa Cruz et al.,2001]. As a consequence, biological corridors mayfacilitate the movement of not only the individualsbetween forest fragments, but also that of native andexotic parasite species [Hess, 1994, 1996], spreadingparasitic infections to healthy isolated groups.

Mantled howler monkeys (Alouatta palliata), oneof the three native primate species of Mexico, areclassified as vulnerable [IUCN, 2002]. Several studieshave identified the presence of endoparasites in howlerpopulations [De Thoisy et al., 2001; Gilbert, 1994;Hugghins, 1969; Kopper-Muller et al., 2000; Mirope-Santa Cruz et al., 2001; Stoner, 1996; Stoner &Gonzalez-Di Pierro, 2005; Stuart et al., 1990, 1998].

In this study we use noninvasive methodologies (1) tocompare gastrointestinal parasite richness, prevalence,and egg density [sensu Bush et al., 1997, number ofparasites in a measured sampling unit taken from ahost] forA. 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, forestfragment shape, forest fragment size, availability offood tree species, and distance to towns on parasiteprevalence. Our objective is to provide a database thatcan be used to make informed recommendations forconservation programs designed to construct forest

corridors between fragmented primate populations.

METHODS

Study Site

The study was conducted between October 2002and April 2003, and included data collected duringboth the wet (OctoberDecember) and the dry(FebruaryApril) seasons. Five rainforest fragments(Fig. 1), located within a total area of 3987 ha in theSanta Marta mountain range, Veracruz (181180Nand 941500 W), were selected for study. These frag-ments have an arboreal stratum 410m and havebeen isolated for 3040 years. The general vegetation

and site characteristics of the Santa Marta mountainrange have been reported elsewhere [Arroyo-Rodrguez et al., 2008; Rodrguez-Toledo et al.,2003]. The human population in the area surround-ing the patches is about 1,200, and all fragments arebordered by pastures [Robles-Martnez, 2009].

Previous research indicated that these frag-ments rank as high-priority targets for conservationbecause they offer adequate patch size for howlers,because of the number of primates living in them,and the possibility of creating biological corridors toconnect them [Rodrguez-Toledo et al., 2003]. Frag-ment size and howler density are reported in Table I.

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Fig. 1. Map showing the forest fragments studied on the Santa Marta mountain range landscape in Veracruz. Areas with diagonal linesare towns (Magallanes, population 243, is given as an example). Lined patches are not occupied by howler monkeys; black patches areoccupied by howler monkeys; the fragments studied are in black and labelled AE (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

Fragment Size (ha) ShapeTBA-foodtrees (m2)

Distance tonearest town (m) No. howlers

Density(ind/ha)

No. fecescollected

A 6.57 2.22 1.16453143 611 5 0.76 30B 9.65 1.48 2.99099955 2,000 8 0.83 48C 11.86 1.47 0.49628248 0 13 1.10 85D 30.06 4.32 2.83891725 560 11 1.20 85E 57.18 2.88 3.49037258 330 6 0.11 30

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Attributes of the Forest Fragments

The landscape characteristics of the SantaMarta mountain range forest fragments have beenreported elsewhere [Arroyo-Rodrguez et al., 2007,2008]. Briefly, the landscape has been digitized

with ArcView 3.2 (Environmental System ResearchInstitute, Inc., Redlands, CA) using aerial photo-graphs (1:20,000), orthophotos, digital data, and fieldinformation [Arroyo-Rodrguez et al., 2005]. Size,distance to the nearest village, and shape for allpatches (Table I) were calculated using the Patch

Analyst 2.2 extension. The shape index of each patchis calculated as SI5P/OAp; where P is the perimeterand 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 isthought to cause fewer edge-related effects forpopulations inhabiting these areas.

Information on food tree species in each frag-ment was collected between January 2004 and May2005, following Gentrys [1982] protocol on tentransects (502 m) randomly placed in each frag-ment as previously reported [Arroyo-Rodrguezet al., 2007]. All tree, shrub, and liana species withdiameter at breast height (dbh) Z10cm wererecorded. Plant species that constitute 480% oftotal howler feeding time at Los Tuxtlas [Fig. 1;Cristobal-Azkarate & Arroyo-Rodrguez, 2007] wereconsidered 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 onceper month, immediately upon defecation. Collectiontook place during the same week and fragments werevisited in a random order. As we could not individuallyrecognize each of the animals, samples from eachgroup were collected early in the morning of a singleday, moving along the group so as not to repeatedlysample the same individual. This methodology hasbeen used previously by other authors studyingparasite loads in primates, and is designed tocalculate an index of parasite prevalence [Chapmanet al., 2005, 2006a; Gillespie & Chapman, 2008]. Asthe number of howlers in each fragment differed, a

different number of samples were collected in each(Table I). Given that the howlers were unable totravel between forest fragments, the parasite infor-mation presented in this study is fragment specific.

Feces were preserved in vials with 5% bufferedformalin and transported to the Instituto de Biologa,UNAM where endoparasite eggs and oocytes wereseparated using sodium nitrate flotation and ethersedimentation methods [Sloss et al., 1994]. The color,shape, and size of the eggs and oocytes were used toidentify the parasite species, and egg density wasobtained using a McMaster counting chamber.Densities are reported as no. of eggs/g of feces.

Data Analysis

Many factors can affect the number of eggsproduced by parasites and contained in the host fecalmaterial [Gillespie, 2006]. Also, Stuart et al. [1990]found that although 100% of A. palliata (N5155) at

their study site in Costa Rica was infected withT. minutus (as evidenced by peri-anal examination),eggs were present in only 22% of the fecal samplescollected, therefore we used samples collected overthree consecutive months to describe each seasonand reduce measurement error.

For each parasite the square root arcsine trans-formed index of prevalence and log-transformedegg parasite density were compared by fragmentand by season with two-way analyses of variance(ANOVAs). The prevalence of multiple infectionswas analyzed with a two-way ANOVA as well. Inorder to have an equal number of replicates per cellfor optimum power [Zar, 1974], a random selection ofthe samples analyzed in the lab was used in thestatistical analyses of egg density.

Using generalized linear models [GLM; Crawley,2002] we selected the combination of two predictorsthat best explained the square root arcsine trans-formed index of prevalence for each parasite. Wecould only use two predictors because we only hadten data on prevalence (two per patch). Thepredictors used were monkey density (to evaluatedensity dependence); food resource availability (mea-sured as TBA of howler food species); distance to thenearest town; and size and shape of the forestfragment (as a measure of habitat quality). We used

a separate slope model with a normal distributionand a log-link function, and tested for collinearitybetween predictor variables [Chatterjee et al., 2000].Sampling season was included as the categoricalvariable in the model.

All analyses were run with STATISTICA 7.1(StatSoft, Inc 19842006).

Ethics

This research adheres to the American Society ofPrimatologists (ASP) Principles for the EthicalTreatment of Nonhuman Primates. Research proto-

cols reported in this manuscript were approved bythe National Wildlife Commission of SEMARNAT(Mexican Secretary for the Environment and NaturalResources), and adhered to the legal requirements ofMexico.

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 threespecies: one unidentified Eimeriidae protozoan(probably Isospora arctopitheci, Michael Stuart,

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but it was higher in the wet months (27.22%) thanduring the dry ones (10.36%).

The density of eggs in feces for all parasitespecies (Table II) differed between fragments(Eimeriidae sp., F57.83, df54, P50.00001;

T. minutus, F5

4.40, df5

4, P5

0.0025; C. biliophilus,F55.52, df54, P50.0004) and seasons (Eimeriidaesp., F529.83, df51, P50.0000003; T. minutus,F520.77, df51, P50.00001; C. biliophilus, F56.05,df51, P50.015). The Tukey post hoc test showed

that in fragment E (the largest), the density ofT. minutus (lowest) and C. biliophilus (highest) differedfrom that of fragments A and B in both cases. And alsofrom fragment C, only in the case of C. biliophilus.Meanwhile values were intermediate for the Eimeriidae

sp. in that largest fragment, compared with the otherfragments (higher: A and B, lower: C and D). Thedensity of Eimeriidae sp. and T. minutus eggs werehigher during the wet season while C. biliophilusdensity was higher during the dry season.

The generalized linear models for the prevalenceof each parasite are listed in Table III. Eimeriidae sp.prevalence was best explained by host density anddistance to the nearest town although only thesecond predictor was significant during the dryseason. The model for T. minutus prevalenceincluded fragment shape and size as the bestpredictors during both seasons. C. biliophilus pre-valence was associated with distance to the nearest

town and the TBA of top food species, but during thewet season only the latter predictor was significant.

DISCUSSION

Although the endoparasite species richness ofhowler monkeys (A. palliata) did not vary across thefive isolated forest patches in this fragmented land-scape, parasite prevalence and egg density were

TABLE II. Egg Density of Parasite Species (egg/gr,mean7standard error) Recorded from Feces of Alouatta palliata Inhabiting Forest Fragments atSierra de Santa Marta Mountain Range. Egg CountDone with a McMaster Counting Chamber

Eimeriidae sp. T. minutus C. biliophilus

FragmentFragment A 111.36721.30 109.09715.30 56.8273.74Fragment B 113.64720.06 88.64710.88 54.5573.14Fragment C 52.2772.27 79.5576.29 56.8273.74Fragment D 54.5574.55 79.5578.49 77.27710.77Fragment E 79.5578.49 54.5573.14 81.8276.19Season Wet 108.18711.84 100.9177.77 59.0972.90Dry 56.3672.59 63.6473.27 71.8274.94

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

Effect Estimate Standard error w2

P

Eimeriidae sp.Intercept 2.64207 0.399637 43.70751 0.000000Wet seasonHowler density 1.10949 0.310474 12.77009 0.000352Dry seasonHowler density 0.55619 0.526119 1.11759 0.290439Wet seasonD. nearest town 0.00047 0.000141 10.95668 0.000933Dry seasonD. nearest town 0.00045 0.000218 4.26707 0.038858 Wet season 0.93744 0.435178 4.64038 0.031228Dry season 0.00000Scale 0.02601 0.005815 20.00000 0.000008

T. minutusIntercept 2.58447 0.159395 262.9012 0.000000Wet seasonFragment size 0.01211 0.002677 20.4573 0.000006Dry seasonFragment size 0.05286 0.010949 23.3092 0.000001

Wet season

Fragment shape 0.09443 0.039116 5.8281 0.015772Dry seasonFragment shape 0.41205 0.108015 14.5520 0.000136 Wet season 0.63094 0.178164 12.5412 0.000398Dry season 0.00000Scale 0.01020 0.002281 20.0000 0.000008

C. biliophilusIntercept 2.77268 0.173923 254.1463 0.000000Wet seasonD. nearest town 0.00022 0.000132 2.8636 0.090602Dry seasonD. nearest town 0.00120 0.000260 21.2703 0.000004Wet seasonTBA food trees 0.21077 0.073862 8.1429 0.004323Dry seasonTBA food trees 0.42954 0.056399 58.0057 0.000000Wet season 0.18718 0.270261 0.4797 0.488564Dry season 0.00000Scale 0.01259 0.002814 20.0000 0.000008

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found to differ. Overall, egg density varied seasonallyand the availability of food, host density, fragmentsize and shape as well as the distance to the nearesttown seemed to be associated with parasite preva-lence, each parasite following a different pattern.

We found that the nematode (T. minutus) andthe trematode (C. biliophilus), previously reportedfor A. palliata in southern Mexico [Trejo-Macaset al., 2007] and Costa Rica [Chinchilla et al., 2005;Stuart et al., 1990], were also present in our studypopulation. Trypanoxyuris also has been found inseveral species of Alouatta in Brazil, Colombia, andSurinam [Stuart et al., 1990, 1993, 1998]. We alsofound an Eimeriidae coccidian which may correspondto I. arctopitheci previously reported for A. palliatain Costa Rica [Stuart et al., 1990], A. pigra inChiapas, Mexico [Stoner, 1996] and A. villosa inPanama [Hendricks, 1977].

T. minutus and the Eimeriidae sp. have a direct

life cycle. Adult T. minutus live in the colon [Muller,2007] and the Eimeriidae sp. develop within the endo-thelial cells of the gastrointestinal tract [Duszynskiet al., 1999]. Both produce oocysts that leave the hostvia the feces and immediately infect the next host toingest them from contaminated food or water. Incontrast, C. biliophilus has a very complex cycle thatrequires two intermediate hosts. The first is believedto be a snail and the second is hypothesized to beants [Vitazkova & Wade, 2006].

The number of parasite species found is consis-tent with previous reports for other howlers studiedin the state of Veracruz. [Canales-Espinosa, 1992;

Lamothe-Argumedo et al., 1997; Villanueva-Jimenez,1988]. However, the species of parasites differed. Incontrast, Trejo-Macas et al. [2007] report up to sixparasite species (three trematodes, two nematodes,and one species of Coccidea) in A. palliata, in a large-scale survey of protected continuous and fragmentedforests in Veracruz, Chiapas and Campeche, Mexico.These authors suggest that the parasite richnessreported for primate groups from protected andcontinuous forests more closely resembles naturalparasitehost ecological relationships than thosefound in primates inhabiting more fragmented land-scapes. This supports the idea that human pressuresthat 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 tobenefit parasites with direct cycles by increasing hostcrowding and reducing competition with indirect lifecycle parasites [Trejo-Macas et al., 2007].

In this study of five forest fragments we found ahigher prevalence of parasites with both a direct(T. minutus) and an indirect (C. biliophilus) life cyclethan those reported for howlers inhabiting protectedand less isolated forests [Chinchilla Carmona et al.,2005; Trejo-Macas et al., 2007]. Parasites do notusually cause the death of the host; however, thedeath of a male A. guariba that had a hyper-infection

of T. minutus [Amato et al., 2002] is a warning thatwhen the physical condition of the host is poor due tofood shortage [Chapman et al., 2006b] or physiologi-cal stress [Martnez-Mota et al., 2007], parasiteinfection may result in death.

We also recorded something that has not beenreported for A. palliata living in continuous, protectedforests: a higher prevalence (29%) of coccidian para-sites at our study site; even higher than that reportedin other fragmented forests [9%, Trejo-Macas et al.,2007]. This is of particular concern because coccidiosisis a major health hazard for domestic and wild animalsunder crowded conditions [Duszynski et al., 1999;Foreyt, 2001] and in high humidity [Moreno-Daz &Ibarra-Velarde, 2002]. Where there has been defor-estation, domestic and wild animals come into contactmore frequently because of forest edge effects[Chapman et al., 2006b]. I. arctopitheci is recognizedas a unique coccidian due to the unusually wide range

of hosts that it can infect. It has been reported inseveral primate species [the tamarin, Saguinus geof-froyi, the capuchin, Cebus capucinus, the nightmonkey, Aotus trivirgatus, the spider monkey, Atelesfuscipes, the howler,A. pigra, and the squirrel monkey,Saimiri sciureus; Duszynski et al., 1999], as well as inthe domestic cat and dog, several wild carnivores, theopossum and humans [Hendricks, 1977]. Cross-infec-tion is probably more frequent in the forest fragmentswhere 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 theprevalence of coccidiosis in domestic animals for theSanta Marta mountain range area; however, it isknown to be a significant problem for sheep, cattle, andpoultry farmers in the state of Veracruz [Moreno-Daz& Ibarra-Velarde, 2002].

The prevalence of the nematode T. minutus wasfound to differ across forest fragments and betweenseasons. Prevalence was lowest in the largest frag-ment (in contrast to the smallest and least circularones) and during the dry season. Troop membershiphas previously been described as the principal factorfor predicting infection with T. minutus in A. pigra[Vitazkova & Wade, 2007]. Some authors also state

that the infectious form in nematodes only developsunder special conditions [Chinchilla Carmona et al.,2005], and high humidity may be one of them.

In contrast, there was no relationship betweenthe prevalence of the other two parasites or multipleinfections and the fragment characteristics or seasonof the year. Some authors have emphasized theimportance of multiple infection indices as a measureof environmental health [Chapman et al., 2006a,b;Trejo-Macas et al., 2007]. Prevalence and eggdensity of multiple infections are higher for redcolobus ( Piliocolobus tephrosceles) inhabiting frag-mented forests than those inhabiting nonfragmented

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ones [Gillespie & Chapman, 2008]. In addition,multiple infections are more prevalent in colobusliving at the forest edge than in those living in theinterior of the fragment [Chapman et al., 2006a]. Inour study, the prevalence of multiple infection

ranged from 0 to 45% and contrasts with the absenceof multiple infection reported by Trejo-Macas et al.[2007] in their broad-scale survey of parasites in A. palliata from fragmented and conserved forests.

We found that fragment traits explain parasiteprevalence but the explanatory trait differed for eachparasite. This is most likely associated with theparasites cycle and the conditions needed for trans-mission. For example: the availability of food treespecies was directly associated with the prevalence ofC. biliophilus. This might result from the greateramount of food trees that are found in forests of betterquality which, in turn, may allow the presence of theintermediate hosts (snails and ants) needed for the

development of this parasite. This hypothesis is alsosupported by the significant association with thedistance to the nearest town, suggesting that lessdisturbance is associated with higher prevalence.During the wet season, however, prevalence is onlyassociated with the availability of top food species.

For T. minutus, larger fragments and irregularfragment shapes were associated with lower pre-valence. This may be due to the fact that, in ourstudy, larger fragments corresponded to those withthe more irregular shapes. This means that a largesize in a fragment minimizes edge-related effectscaused by irregular forest peripheries.

Harder to explain is the model found for theprevalence of Eimeriidae sp., given that an inverserelationship was found with host density and a directone with distance to the nearest town. Coccideanparasites are closely associated with crowded condi-tions [Duszynski et al., 1999; Foreyt, 2001] but thisdoes not seem to apply in this study. However, thehigher prevalence in fragments farther away fromtowns may indicate that their presence requires less-disturbed localities where other wild, free-ranginghosts may be present as well [Hendricks, 1977]. Asmentioned above, the forest fragments studied (andthe larger ones probably more) are inhabited byseveral 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, thefragments that are located farther from towns arenot the largest, nor are they the least crowded. Thisreduces the chances of detecting clear relationships.The aim of our study was to reveal the role ofseasonality and this made it necessary to use a smallnumber of fragments. A broader survey duringdifferent seasons may further clarify the trendsobserved here. However, our findings in this studyof A. palliata and its parasites in the fragmentedlandscape of the Santa Marta mountain range do

seem to support the idea that habitat transformationchanges hostparasite dynamics [Altizer et al., 2003;Nunn et al., 2003], parasite virulence and parasitehost range [Daszak et al., 2000].

Seasonal variation in parasite infection needs to

be evaluated for any population to be included inconservation management practices. Egg density forall parasites varied with season and fragment.Density for both of the parasites with a direct lifecycle, the Eimeriidae sp. and T. minutus, was higherduring the wet season, whereas density forC. biliophilus was higher during the dry season. Highvalues of C. biliophilus during the dry season havebeen previously reported in A. pigra, but as elevatedprevalence [Vitazkova & Wade, 2007]. The largestforest fragment was characterized by an intermediatedensity of the Eimeriidae sp., a higher density ofC. biliophilus, and lower egg density for T. minutus.

In conclusion, the conservation and management

practices of threatened and endangered primatesmust take into account the effects of environmental,demographic, behavioral, and human trends whenassessing infection rates [Stuart & Strier, 1995]. Inthe Santa Marta mountain range we found that para-site richness does not differ among howler groupsliving in different forest fragments. This suggeststhat the proposal of setting forest corridors topromote primate dispersal and gene flow [Escobedo-Morales & Mandujano, 2007; Rodrguez-Toledo et al.,2003] could be innocuous. However, lower parasitespecies richness than that of howlers in protectedforests, as well as differences in the prevalence and

egg density of the parasites recorded among thefragments warn us to be cautious when designingthese corridors. For example, increased connectivitybetween fragments could reduce global prevalence ofT. minutus, as this species was least prevalent in thelargest fragments. However, it may as well result inthe increased prevalence of Eimeriidae sp. becausethe other wild hosts will also be able to movealong the corridors. Human induced migration andcontact between two different colobus species (thered colobus, P. tephrosceles and the black-and-whitecolobus, Colobus guereza) has already resulted in theincreased prevalence of parasites that seem to haveled to a decline in the black-and-white colobus

population [Chapman et al., 2005]. Therefore, ifeffective conservation policies are to be put intopractice epidemiological information should be takeninto account. For example, an initial increase in thearea of each fragment (by reforesting the perimeter)could even out parasite infection in all of thefragments to be connected. Also, as this and otherstudies [Chapman et al., 2006b] have demonstrated,food availability is an important factor in determin-ing parasite prevalence. Reforestation with treespecies used by the howlers as food could accelerateevenness in parasite infection before the corridorreforestation solution is put into practice.

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ACKNOWLEDGMENTS

We thank Ruben Mateo and his family forassistance in the field and for storing the samples.Guillermo Salgado and David Osorio gave advice andassistance in the laboratory. Dr. Michael Stuart

corroborated our identification of parasites and gavea taxonomic position for the Coccidean parasite.Dr. Vinicio Sosa helped with the statistical analysis ofthe data and Rodolfo Martnez-Mota revised an earlierversion of this manuscript. Bianca Delfosse improvedthe English. This research complies with protocolsapproved by the National Wildlife Commission ofSEMARNAT (Mexican Secretary for the Environmentand Natural Resources), and the legal requirements ofMexico.

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Gastrointestinal parasites of howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Sierra Santa Marta mountain range, Mexico