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Parasitos intestinales de Alouatta caraya (primates, ceboidea): estudio preliminar en semi cautiverio y en vida silvestre en la Argentina.



Parasites represent an important and ubiquitous component of primates natural communities (Nunn et al, 2003; Nunn and Altizer, 2006; Vitazkova and Wade, 2006). Primates are particularly vulnerable to the infections of directly transmitted parasites because they often live in close social groups that facilitate their transmission (Stoner, 1996; Stoner et al., 2005). The genus Alouatta is the most widely distributed of the New World monkeys, ranging from 18[grados] N in Mexico to 27[grados]S in Argentina, where the black and gold howler monkey, Alouatta caraya (Humboldt, 1812), reaches the southernmost limit of its geographic distribution in the provinces of Formosa, Misiones, Chaco, Corrientes and Santa Fe (Neville et al., 1988; Brown and Zunino, 1994). Among Neotropical primates, species of the genus Alouatta are some of the best studied in relation to parasite infections. For example, Stuart et al., (1990) found a high incidence of Strongylid infections in troops of A. palliata inhabiting riverine forests in Costa Rica, suggesting that high humidity would prolong larval survival. In Mexico, Trejo-Macias et al. (2007) identified six species of intestinal parasites (two unidentified trematodes, Controrchis biliophilus, Trypanoxyuris sp., Parabronema sp. and one Coccidia) in troops of A. p. mexicana inhabiting continuous and fragmented forests and found a higher prevalence of infection in fragmented habitats, related to a greater contamination from humans and domestic animals. For A. pigra, 16 species of endoparasites were reported in Belize and Mexico; six protozoans, six nematodes, two trematodes and two cestodes (Stoner and Gonzalez-Di Pierro, 2005; Eckert et al., 2006; Vitazkova and Wade, 2006, 2007; Trejo-Macias et al., 2007), and in general they found an increased prevalence of nematodes and some protozoan during the wet season and in fragmented habitats. In the case of A. seniculus, Phillips et al. (2004) provided baseline information on the presence of three protozoan (Chilomastix mesnili, Blastocystis hominis and Iodamoeba buetschii) and two helminths (Strongyloides sp. and Trichuris sp.) in south-eastern Peru. Martins et al. (2008) surveyed troops of A. belzebul at five sites in the Brazilian state of Para recovering 12 taxa of endoparasites, being relatively high the infection rates, and showing a marked variation both within and among populations. Finally, almost 11 endoparasites species were identified from A. guariba in forest patches next or within plantations and in close proximity to human settlements in different regions in Brazil, suggesting these factors increases the human-wildlife parasites exchange (Kowalewski and Gillespie, 2009).

Field studies conducted on wild populations of A. caraya in Argentina have provided information on different groups of intestinal parasites infecting this species such as nematodes, Trypanoxyuris sp., Trypanoxyuris minutus, Strongyloides sp.; unidentified Trematoda eggs and Bertiella mucronata (Cestoda) (Santa Cruz et al., 2000 a; b; Delgado, 2006; Kowalewski et al., 2010). Giardia lamblia (Syn. G. intestinalis [Lambl, 1859]; G. duodenalis Stiles 1902) was the only protozoan reported (Venturini et al., 2003; Kowalewski et al., 2010). A. caraya faces changes in its natural habitat such as, deforestation as well as illegal hunting, because it is the most commonly traded primate for the pet market in Argentina (Bertonatti, 1995; Chebez, 2009). The study of infection patterns in semi captive primates may help to provide an index on the health status of individuals. Coprological surveys for intestinal parasites involve non-invasive procedures and provide data to be included in the analysis of ecological relationships between primates and their environment (Eckert et al., 2006; Gillespie, 2006).

In the framework of the study of behavior and intestinal parasites of black and gold howler monkeys, our main objective was to describe the intestinal parasites in semi captive and wild howler monkeys A. caraya troops (ACA) from the Centro de Reeducacion del Mono Aullador Negro (CRMAN) and campo Las Lomas, respectively in Argentina.


Study sites

In the present study, we surveyed four howler monkeys A. caraya troops. Two of the troops were held in semi captivity at the CRMAN; this 300 ha private-owned land is located in La Cumbre (30[grados] 59' S; 64[grados]29'W), Cordoba Province, at 1420 m asl, in central Argentina. The local climate is temperate, with temperatures ranging from -8.8[grados]C to 32[grados]C in winter and 0.8[grados]C to 38.4[grados]C in summer; the average annual rainfall is 700 mm (Demaio and Medina, 1999). The landscape is a combination of native hilly forest (locally called "bosque serrano") and a matrix of grassland (Festuca sp. and Stipa sp.). In addition, the area has been extensively altered by human activities resulting in a modification of the natural forest and the introduction of exotic vegetation, which is suitable habitat for howler monkeys (Bruno et al., 2005; Bruno, 2011; Bruno and Mudry, 2011). The other howlers under study were two wild troops from campo Las Lomas, a 623-ha private-owned land, located in San Cosme District, Corrientes province, in the northeast of Argentina (27[grados]23'S; 58[grados]22'O). The local climate is subtropical, with a mean annual temperature of 21[grados]C and an average annual rainfall of 1200 mm (Rumiz et al., 1986). The landscape is characterized by a semi deciduous forest surrounded by a matrix of grassland (Carnevalli, 1994; Burkart et al., 1999; Zunino and Kowalewski, 2008). There are several seasonal lagoons surrounding some of the forest patches.


We surveyed four troops of howler monkeys, two held in semi captivity (T2: 4 adults, 1 subadult, 2 juveniles and 2 infants; and T3: 4 adults, 1 subadult, 5 juveniles and 3 infants) and two wild troops (T. Sopranos: 4 adults, 1 subadult, 4 juveniles and 3 infants; and T. Mudo: 8 adults, 3 juveniles and 2 infants). We identified the howler monkeys based on body size, coat color, natural markings, wounds and facial features (Cabrera, 1958). At campo Las Lomas, we habituated the howlers to our presence during a three-month period. The CRMAN receives and houses illegally commercialized howler monkeys and particular donations (Bruno et al., 2005). After arrival, the individuals received veterinary assistance (including treatment for parasitic infections when needed). The monkeys are maintained in facilities for two to six years, and subsequently groups are formed and released in the forest patches (Bruno et al., 2005). Once released, they are only provided with a daily ration of supplementary food and fresh water, besides the natural vegetation of the patches (Bruno, 2011; Bruno and Mudry, 2011). We selected these two troops because their conformation is stable, and since the controlled release no management is involved except for the recapture of expelled or sick individuals. T2 was formed in 2000 and released in January 2001 and T3 was formed and released in 2003 (Bruno, 2011). Once released, the individuals did not receive any parasitic treatment.

Sample collection and analysis

We followed each troop from dawn to dusk and collected serial samples of fresh feces from 38 individuals of the four troops immediately after defecation to avoid contamination (preferably in the morning). We collected three fecal samples from each individual, resulting in a total of 110 samples. All fecal samples were taken from individually identified monkeys and stored in flasks containing 10% formalin solution. We processed all the samples in the CEPAVE-UNLP (Centro de Estudios Parasitologicos y de Vectores. Universidad Nacional de La Plata) via standard concentration by sedimentation (Ritchie, [delta]=1010) and by flotation (Sheather, [delta]=1200) techniques (Becerril Flores and Romero Cabello, 2004). The samples resulting from the application of these techniques were divided among three different slides, each for a different method, in order to search for parasitic forms (eggs, cysts and larvae), using temporary staining (Lugol's iodine), and examined under light microscopy at 100, 400 and 1000 x magnification (Olympus BX 51). Parasites were identified based on morphology, size, and appearance of eggs, cysts and larvae following standard references. We described parasite infections in terms of prevalence of infection and species richness. Prevalence is the proportion of individuals hosts sampled infected with a particular parasite species (Stuart and Strier, 1995; Bush et al., 1997; Gillespie, 2006; Chapman et al., 2009). Richness (S) is defined as the number of unique intestinal parasitic species documented from the host's fecal samples (Chapman et al., 2006). Sorensen Similarity Coefficient (CS) was also calculated to assess parasite species composition between study sites (Morales and Pino, 1987). We calculated prevalence of infection for total intestinal parasite species and for each individual parasite species in howler monkeys for each study site. We performed a [ji al cuadrado] test to compare variations in parasite prevalence between the two study sites, with EPIDAT 3.1 and PASW Statistic 18 software. Statistical significance was assumed at [alfa] < 0.05.


Species composition and total prevalence of howler parasites at CRMAN and Las Lomas

Howler monkeys were parasitized by six parasite species. Infections of protozoa included one nonpathogenic amoeba (Entamoeba coli), Blastocystis hominis, Giardia lamblia, and Eimeria sp. Helminths recovered included eggs of the cestode Bertiella mucronata, and the nematode larvae of Strongyloides sp. (Table 1). Of all individuals examined from both areas, 86.8% (33/38) were infected with at least one type of gastrointestinal parasite. In the CRMAN, the prevalence was lower (72.2%), whereas all individuals from Las Lomas were infected (100%). Protozoa were found in 78.9% of the animals; 55.5 % in the CRMAN and 100% in Las Lomas. Helminths were less prevalent and were found in 21% of all howlers sampled, 22.2% in the CRMAN and 20% in Las Lomas. In the present study, the two most prevalent species were Blastocystis hominis (73.7%) and Giardia lamblia (50%). Species richness (S) was higher in wild troops in Las Lomas (6 vs. 4) and parasite species composition in both areas showed a similarity of 80% (CS = 0.80).

Comparison of parasite prevalence between howlers from CRMAN and Las Lomas

The total prevalence of intestinal parasites was higher among howlers from Las Lomas than those of the CRMAN, and two species, Eimeria sp. and Strongyloides sp. were found only at Las Lomas. However B. mucronata, was more prevalent among howlers from the CRMAN (Table 1). Significant differences in prevalence of infection was found between sites for three species of protozoan (Blastocystis hominis: [X.sup.2] = 21.37, p < .05; G. lamblia: [X.sup.2] = 18.24, p< .05 and Entamoeba coli: X[.bar]2 = 50.09, p < .05) which were more prevalent at Las Lomas.


To our knowledge, this is the first report on gastrointestinal parasites from semi captive troops of howler monkeys A. caraya in Argentina. Five of the gastrointestinal parasites species identified in the four troops surveyed have been reported in previous studies for A. caraya in Argentina and Brazil: Blastocystis hominis in Corrientes, Argentina (Martinez et al., unpublished); Giardia lamblia also in the same region (Venturini et al., 2003; Kowalewski et al., 2010) and Eimeria sp. in Brazil (Godoy et al., 2004). Among helminths, the nematode Strongyloides sp. was described in Corrientes (Santa Cruz et al., 2000a), as well as the cestode Bertiella mucronata, which was also reported from Corrientes and Chaco, Argentina (Santa Cruz et al., 2000 a, b). In the present study, we found more species (six) of gastrointestinal parasites than previously reported in Argentina (Pope, 1966 [two species]; Santa Cruz et al., 2000b [two species identified]; Venturini et al., 2003 [one specie]; Delgado, 2006 [two species] and Kowalewski et al., 2010 [one specie]). However, the lower species richness of parasites in monkeys from the CRMAN compared to those from Las Lomas may be related to the fact that they were captured when they were infants, isolating them from their natural environment and preventing them from natural parasitic infection. Another possible explanation may be related to the environmental conditions in both study sites.

The prevalence of Giardia lamblia in wild howlers from Las Lomas was similar or higher than previous records for the same region (70 % vs 67 %) (Kowalewski et al., 2010) and from wild troops in Chaco, where Venturini et al. (2003) found only 3.6 % of infection and Kowalewski et al. (2010), 57 %. The prevalence of Bertiella mucronata found in wild howlers in our study, showed a higher prevalence of infection compared to findings by Delgado (2006) (20 % vs 5 %), but similar ( 20 % vs 21%) compared with Santa Cruz et al. (2000b) in wild troops from Isla Brasilera, Chaco.

We found no evidence of infection with Cryptosporidium sp. However, there is one record of Cryptosporidium sp in one howler monkey kept in semi captivity in Corrientes (Santa Cruz et al., 2002). In this regard, Kowalewski et al. (2010) suggested this pathogen is not a natural component of the howler parasite communities in Chaco and Corrientes. The results of our study based on the analysis of 110 samples over a period of one year could support the findings by Kowalewski et al. (2010).

We found significant variation in parasite prevalence between howlers from the two study sites. Protozoan infection was higher in wild monkeys from Las Lomas than those in semi captivity from the CRMAN. This could be related to the environmental differences between the two areas, where warmer and wetter regions (characteristic of Las Lomas) are more favorable for the survival of infectious stages of some parasitic species, thus increasing chances of infection. Factors such as high precipitation, humidity and low altitude seem to be associated with higher levels of parasite prevalence and richness (Stuart et al., 1998; Stoner et al., 2005; Kowalewski and Gillespie, 2009). Many of the frequently studied parasites of primates are transmitted orally, either when the monkey ingests contaminated water, plant foods, or by an intermediate host containing the infective stage of a parasite (Nunn and Altizer, 2006; Chapman et al., 2009). Natural infection by protozoans seems to occur through the ingestion of resistant cyst (Nunn and Altizer, 2006), which are found in soil, food, water or surfaces contaminated with feces from infected animals (Godoy et al., 2004). Among protozoa, Giardia lamblia and Blastocystis hominis are potential zoonotic gastrointestinal parasites (Kowalewski and Gillespie, 2009). Giardia lamblia is commonly found in Alouatta, while Blastocystis hominis was found in Alouatta seniculus (Stuart et al., 1990; Phillips et al., 2004: Chinchilla et al., 2005), A. pigra (Stoner and Gonzalez-Di Pierro, 2005) and A. caraya. Blastocystis hominis and Giardia lamblia were present and prevalent in howlers from both study sites. It is important to note that the most prevalent parasites have a direct life cycle, which would facilitate their transmission. Most of the species of parasites found in the present work also parasitize humans and livestock (Nunn and Altizer, 2006; Kowalewski and Gillespie, 2009; Vitazkova, 2009), and the fact that the howlers surveyed inhabit environments with frequent contact with human communities, may increase opportunities to cross-species transmission (Kowalewski and Gillespie, 2009). In addition, the permanent presence of humans and frequently concurrence of tourism in the case of the CRMAN and the regular presence of poachers (illegal hunters) and rural workers in Las Lomas, may contribute to human-wildlife disease exchange, and howler monkeys may serve as reservoirs for human infection.

Helminths are also commonly reported in wild primates (Nunn and Altizer, 2006). The occurrence of Bertiella mucronata in A. caraya has been previously reported in Argentina, (Pope, 1966; Santa Cruz et al., 1995; Santa Cruz et al., 2000 a, b). According to Stuart et al. (1998) the infection is probably related to the accidental ingestion of oribatid mites bearing cysticercoids. Howler monkeys are primarily folivorous, and there are no reports that they deliberately consume arthropods. The low prevalence of infection of B. mucronata in our study may be a result of the low consumption of invertebrates in their diet. However, Bravo and Zunino (1998) found the presence of arthropod larvae within some of the seeds consumed by A. caraya. It is likely that howler monkeys may become infected when accidentally ingesting the intermediate hosts while foraging on leaves, fruits, or drinking contaminated water. The higher prevalence of B. mucronata in monkeys of the CRMAN compared with those from Las Lomas, may be due to environmental factors, such as low relative moisture and higher solar irradiation that could favor the persistence of intermediate hosts. Also, howlers could be ingesting the infected arthropods accidentally during terrestrial travel. We registered frequent terrestrial locomotion and travel, often over defecation sites, only in howlers from the CRMAN, thus increasing the opportunity for transmission of the infective stage. Strongyloides sp. occurs in tropical and subtropical regions, although it can be found in more temperate ones, where is associated with wetter areas (Nunn and Altizer, 2006). The larvae are eliminated in the feces as L1 and need humid soils to develop into the infective L3 stage. In our study, Strongyloides sp. was present in wild howlers from Las Lomas, where the high humidity may favor its development.

The results of our study may contribute to the baseline knowledge of intestinal parasites infecting howler monkeys and aid in the understanding of patterns of parasitism in A. caraya. In turn, coprological surveys of endoparasites will allow us to non-invasively estimate the health of individuals, detect the presence of parasites of zoonotic importance and assess whether there is any risk for other wild populations in case of translocation.


This study is a contribution to a baseline knowledge of endoparasites infecting black and gold howler monkeys, A. caraya, in Argentina. We found wild troops of howler monkeys from Las Lomas to have greater species richness of parasites and higher prevalence of protozoan infection. Differences in the microenvironment between the two study sites may account for the variation in parasite prevalence in individuals of A. caraya. Further analysis of the association between socioecological variables and indices of parasite infection will provide valuable information of the patterns of parasitism in semi captive and wild howler monkeys in the two study sites.

Recibido 17 enero 2012. Aceptado 23 marzo 2012. Editor asociado: MR Robles


We thank A. Juarez, director of the CRMAN, for allowing us to use the facilities at the Center, and J. P. Heredia and C. Arnijas for field assistance. We are also grateful to J. Ezcurra, M. Brusca and L. Lagos for allowing us access to their facility in Corrientes and for their support during surveys, and to our field assistants who helped in the collection of fecal samples. We also acknowledge two anonymous reviewers for their helpful suggestions that greatly improved the original manuscript. This research was supported by grants to MDM from UBACyT X-107 and CONICET PIP 5012.



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Carola Milozzi (1,2,4), Gabriela Bruno (1,3), Elisa Cundom (2), Marta D. Mudry (1,4), and Graciela T. Navone (2,4)

(1) Grupo de Investigacion en Biologia Evolutiva (GIBE), Depto. EGE, IEGEBA-CONICET, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Intendente Guiraldes Nro. 2160, 1428EHA Buenos Aires, Argentina. [Correspondence: <>]. (2) Centro de Estudios Parasitologicos y de Vectores (CEPAVE), Universidad Nacional de La Plata-CONICET, Calle 2 No. 13 584, 1900 La Plata, Argentina. (3) Centro de Reeducacion del Mono Aullador Negro (CRMAN), Camino Estancia El Rosario, Ruta E66, Paraje Tiu Mayu, La Cumbre, Cordoba, Argentina. (4) CONICET.
Table 1
Species composition and prevalence of infection
(%) of howler parasites in Argentina.

Parasite species                 Prevalence of infection (%)

                                 CRMAN   Las Lomas   Both sites

Blastocystis hominis             44.4      100.0        73.7
Giardia lamblia                  27.7      70.0          50
Entamoeba coli                    5.5      65.0         36.8
Eimeria sp.                       0.0      15.0         7.9
Bertiella mucronata              22.2      10.0         15.8
Strongyloides sp.                 0.0      10.0         5.3
Total protozoan infection        55.5      100.0        78.9
Total helminth infection         22.2      20.0          21
Number of individuals sampled     18        20           38
Number of samples collected       50        60          110
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Title Annotation:texto en ingles
Author:Milozzi, Carola; Bruno, Gabriela; Cundom, Elisa; Mudry, Marta D.; Navone, Graciela T.
Publication:Mastozoologia Neotropical
Date:Dec 1, 2012
Previous Article:Revision craneo-dentaria de Procyon (Carnivora: Procyonidae) en Colombia y Ecuador, con notas sobre su taxonomia y distribucion.
Next Article:El registro de Megatherium (Xenarthra, Tardigrada) en Mendoza (Argentina): aspectos taxonomicos, cronologicos y paleoecologicos.

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