Primates DOI 10.1007/s10329-014-0413-7
ORIGINAL ARTICLE
Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica Selene Maldonado-Lo´pez • Yurixhi Maldonado-Lo´pez Alberto Go´mez-Tagle Ch. • Pablo Cuevas-Reyes • Kathryn E. Stoner
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Received: 18 April 2013 / Accepted: 2 February 2014 Ó Japan Monkey Centre and Springer Japan 2014
Abstract In primate populations, endoparasite species richness and prevalence are associated with host traits such as reproductive and social status, age, sex, host population density, and environmental factors such as humidity. We analyzed the species richness and prevalence of intestinal parasites in two sympatric primate populations, one of Alouatta palliata and one of Ateles geoffroyi, found in a tropical dry forest in Costa Rica. We identified three species of intestinal parasites (Controrchis sp., Trypanoxyuris sp., and Strongyloides sp.) in these two primate species. We did not find any differences in species richness between the primate species. However, the prevalences of Controrchis sp. and Trypanoxyuris sp. were higher in Alouatta palliata. Similarly, males and lactating females of Alouatta palliata showed higher Controrchis sp. prevalences. We did not observe any differences in parasite richness and prevalence between seasons. Infectious diseases in endangered primate
S. Maldonado-Lo´pez (&) Y. Maldonado-Lo´pez Centro de Investigaciones en Ecosistemas, UNAM, Antigua Carretera a Pa´tzcuaro No. 8701, Col. Ex-Hacienda de San Jose´ de la Huerta, 58190 Morelia, Michoaca´n, Mexico e-mail: [email protected] A. Go´mez-Tagle Ch. INIRENA, Universidad Michoacana de San Nicola´s de Hidalgo, Ciudad Universitaria, 58030 Morelia, Michoaca´n, Mexico P. Cuevas-Reyes Laboratorio de Ecologı´a de Interacciones Bio´ticas, Facultad de Biologı´a, Universidad Michoacana de San Nicola´s de Hidalgo, Ciudad Universitaria, 58030 Morelia, Michoaca´n, Mexico K. E. Stoner Department of Fish, Wildlife and Conservation Ecology, New Mexico State University, MSC 4901, P.O. Box 30003, Las Cruces 88011, New Mexico, USA
populations must be considered in conservation strategies, especially when defining protected areas. Keywords Alouatta palliata Ateles geoffroyi Host sex Host age Endoparasites Tropical dry forest
Introduction Endoparasitic infections are very common in nonhuman primate populations (Stuart et al. 1990, 1998; Stoner 1996; Altizer et al. 2003; Nunn et al. 2003; Stoner and Gonza´lezDi Pierro 2006; Gillespie and Chapman 2008; Valdespino et al. 2010). Many of these parasites act as commensals most of the time, but they are pathogenic when the resistance of the host is depressed or their abundance is unusually high (Amato et al. 2002; Chapman et al. 2006; Martı´nez-Mota et al. 2007). The high species richness and prevalence of endoparasites in wild primate populations are associated with some host traits such as reproductive and social status, age, sex, and host population density (Altizer et al. 2003; Godoy et al. 2004; Eckert et al. 2006; Trejo-Macı´as et al. 2007; Raharivololona and Ganzhorn 2009; Pebsworth et al. 2012; Trejo-Macı´as and Estrada 2012; Vitazkova and Wade 2007). For example, primates that show highly social behavior are more exposed to infective stages of endoparasites (Gilbert 1994). In high-density primate populations, high endoparasite species richness and prevalence might be expected, because the chance that a primate in such a population will be found by endoparasites is greater than the chance that they will be found as an isolated primate. In this case, a response by the endoparasites to the amount of resources available is implied, with host proximity regulating endoparasite population size via density-
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dependent mechanisms (Freeland 1980; Stuart et al. 1990; Altizer et al. 2003; Nunn et al. 2003; Valdespino et al. 2010). In primate species that occur in sympatric conditions, both populations are susceptible to the same parasite species as a result of the proximity of the primates in the neighborhood (Freeland 1983; Stuart et al. 1998). Sex, age, and reproductive status affect the expression of sex steroid hormones (i.e., estrogen, progesterone, and testosterone) (Lamason et al. 2006) that modulate host immunoresponse in animals (Klein 2004). Estrogen stimulates the immune system, while progesterone and testosterone are considered immunosuppressors (Klein 2004; Trejo-Macı´as et al. 2007). Therefore, females might be expected to offer more effective resistance against some parasitic infections than males. However, lactating or pregnant females (O’Sullivan and Donald 1970; Lamason et al. 2006; Stoner and Gonza´lez-Di Pierro 2006), as well as primates with secondary reproductive character development (juvenile stages), have lower resistance to parasitic infections (Lamason et al. 2006; Mu¨ller-Graf et al. 1997; Stoner and Gonza´lez-Di Pierro 2006). In the same way, environmental factors such as humidity can promote the survival, development, and transmission of the infective stages of endoparasites (Stuart et al. 1990, 1993; Jones 1994; Stoner 1996, Bonilla-Moheno 2002; Eckert et al. 2006). Therefore, primates living in humid environments may show higher endoparasite species richness and prevalence (Stuart et al. 1990, 1993; Jones 1994; Stoner 1996, 1996; Stuart et al. 1998; Stoner and Gonza´lez-Di Pierro 2006; Cristo´bal-Azkarate et al. 2010; Valdespino et al. 2010; Trejo-Macı´as and Estrada 2012). It is particularly important to identify the factors that affect parasitic infections in wild primate populations (Gilbert 1994; Stoner 1996; Stuart et al. 1998; Gillespie and Chapman 2008), especially endangered primate species such as Alouatta palliata and Ateles geoffroyi (UICN 2002), which have been displaced to fragmented forests and disturbed areas (Arroyo-Rodrı´guez and Dias 2010; Chaves et al. 2011) in many regions in which they occur. Several studies have described endoparasitic infections of howler monkeys (Alouatta sp.) (Neville 1972; Stuart et al. 1990, 1998; Gilbert 1994; Stoner 1996; Stoner and Gonza´lez-Di Pierro 2006; Valdespino et al. 2010; Trejo-Macı´as et al. 2007; Trejo-Macı´as and Estrada 2012) but only a few studies have documented endoparasitic infections in spider monkeys (Ateles sp.) in the wild (Bonilla-Moheno 2002). Similarly, little information exists about patterns of parasitic infection of sympatric primate species. Stuart et al. (1998) demonstrated differences among primate species in parasite prevalence, with 49 % of Ateles, 51 % of Alouatta, and 91 % of Cebus found to be parasitized. Furthermore, Controrchis biliophilus prevalence was higher in Alouatta than in Ateles or Cebus species.
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In our study, we analyzed and compared the richness and prevalence of the endoparasites in two sympatric monkey populations—one of Alouatta palliata and one of Ateles geoffroyi—inhabiting a tropical dry forest fragment with strong seasonality. We hypothesized that Alouatta palliata and Ateles geoffroyi share the same intestinal parasite species since they are sympatric species that occupy the same home range in the study site (Freeland 1983). However, we expected different percentages of parasitic infection (prevalence) for the two primate species as a result of their intrinsic physiological and ecological differences (Milton 1981; Freeland 1983). Our objectives were (1) to analyze and compare differences in endoparasite richness and prevalence between sympatric populations of A. palliata and A. geoffroyi; (2) to evaluate the importance of host sex, host age, and female reproductive stage (FRE) in endoparasite infections of A. palliata and A. geoffroyi populations; and (3) to analyze the effects of seasonality on endoparasite infection.
Methods Study area This study was conducted in the Tropical Dry Forest of Santa Rosa National Park in Costa Rica, in the Murcie´lago section, Guanacaste Conservation Area, situated in northwestern Costa Rica. This area was declared part of the Santa Rosa National Park in 1980 (Janzen 1986); it is a mountainous area covering approximately 122 km2 with low hills and forests. It is a seasonal forest with a severe dry season from December to May and an annual rainfall of 900–2500 mm (Janzen 1986; Hiramatsu et al. 2008). As a result of livestock, deforestation, and agriculture, the Murcie´lago section currently presents a mosaic of vegetation that includes secondary forests, abandoned pastures, and forest fragments. The populations of Alouatta palliata and Ateles geoffroyi studied occur in sympatry in a forest fragment with deciduous and riparian vegetation. Study species Alouatta palliata This is the only genus of the subfamily Alouattinae of the neotropical family Cebidae (Napier 1976). The genus Alouatta includes six species that are distributed from southern Mexico to northern Argentina (Wolfheim 1983; Crockett and Eisenberg 1987). In particular, A. palliata is found from southern Mexico, possibly southern Guatemala, and from Honduras through Central America to Colombia and western Ecuador (Crockett and Eisenberg 1987). The
Primates
howler monkey has the widest distribution of all the Neotropical primates, and occupies a vast range of habitat types (Crockett and Eisenberg 1987). It is found at elevations of 2,300 m in moist evergreen habitats and in semideciduous habitats with marked seasonality (Mittermeier and van Roosmalen 1981; Crockett and Eisenberg 1987). Alouatta palliata is the largest of the Neotropical primates, with adults weighing from 4 to 10 kg, and it has clear sexual dimorphism, as males can be more than twice as heavy as females. Howler monkeys are primarily folivores, although they can consume a considerable amount of fruit depending on the location or time of year (Reid 1997). Ateles geoffroyi This species has nine subspecies that are separated almost entirely on the basis of fur color (Kellogg and Goldman 1944). The spider monkey is distributed over a vast area in Central America and South America. It is located from the southern River Yapacani in Bolivia to northern Mexico in the eastern coastal state of Tamaulipas. Ateles geoffroyi in central America seems to be more flexible in its habitat selection than most of its South American relatives. In Costa Rica, it has been observed in evergreen, semideciduous, and deciduous forests (Freese 1976). The genus Ateles is primarily frugivorous, selecting the soft parts of a great variety of fruits. Other parts of the plants, such as young leaves, flowers, and bark, are less commonly consumed by the spider monkey (Reid 1997; Di Fiore et al. 2008). They can also passively eat some insects such as larvae and wasps that are usually found in the plant species they consume (van Roosmalen and Klein 1988). Fecal sampling, preservation, and analysis Alouatta palliata and Ateles geoffroyi are threatened species (UICN 2002), and it was necessary to identify endoparasites using a noninvasive procedure that provides data on the richness and prevalence of parasitic infections (Gillespie 2006). Samples from two sympatric troops of primates, one of A. palliata and the other of A. geoffroyi, were collected between May 2000 and March 2001, and included data collected during both the wet (June– November) and dry (December–May) seasons. Troops were followed, and samples were collected at the time of defecation during the morning. Using a spatula, we carefully collected the top and central parts of the fecal sample to avoid contact with the ground and contamination with other organisms. Fresh feces from individual monkeys were stored immediately after defecation in sterile vials with 10 % formalin. The same quantity was collected for each sample by adding feces until the formalin was displaced a given amount. We recorded the date, time of
collection, and identity of the individual observed (name, sex, age, FRE). In total, we collected fecal samples from 134 individuals: 94 samples of A. palliata and 40 of A. geoffroyi. Parasites were identified by the presence of eggs and larvae in the feces. To determine the species richness of endoparasites and their prevalence in the hosts, we performed two different analyses (i.e., qualitative and quantitative). In the qualitative analysis, the presence of eggs and larvae were determined by direct microscopic observation of the samples. For each sample we prepared two slides, and in each one we deposited two sample drops and one drop of Lugol’s iodine solution under a coverslip (24 9 50 mm). We systematically observed the entire slide under 209 and 409 objectives and taxonomically identified each endoparasite species. In the quantitative analysis, the number of eggs and larvae was determined after sample sedimentation using a formalin-ethyl acetate centrifugation technique (Long et al. 1985). After centrifugation, two drops of the prepared sample and one drop of Lugol’s iodine solution were placed on a microscope slide with a glass coverslip (24 9 50 mm). Four slides of each sample were examined systematically with a compound microscope. Parasites were identified on the basis of egg and larvae morphology and size, measured at 4009 to the nearest 0.1 lm with an ocular micrometer. Most studies that have evaluated parasite–primate interactions have assumed that parasite species richness can be estimated using a single slide per sample (Stuart et al. 1990). However, in a preliminary analysis, we found that parasite species richness is underestimated when it is analyzed using a single slide per sample rather than four slides per sample, indicating that parasite richness can vary significantly in accord with the number of slides analyzed in the study. Therefore, we decided to examine four slides per sample in our study. Statistical analysis In order to determine the differences in infection prevalence between the monkey species and between seasons, we conducted a single logistic regression analysis using the GENMOD procedure (SAS 2000). The analysis incorporated host species, month nested in season, and the interaction between host species and season as independent variables and the percentage of infected individuals as the response variable. In the analysis we used a binomial distribution (presence–absence) and a logit link function. To determine if some combinations of parasite species (co-infections per pair of parasite species) are more or less likely to occur than expected from their prevalence alone in the host primate species, we used Fisher’s exact test.
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To analyze the differences in parasite prevalence between host sex, host age, and FRE in A. paliatta and A. geoffroyi, we performed a logistic regression analysis using the GENMOD procedure (SAS 2000) for each parasite species. The model used host sex, host age, and FRE as independent categorical variables and the percentage of infected individuals as the dependent variable. In the analysis, we used a binomial distribution and a logit link function.
and their widths were 20–22.5 lm (n = 20, average = 21.4 lm, SD = 0.83). The germinal masses were visible below the operculum in most of them (Fig. 1a). Trypanoxyuris sp.
Results
The genus Trypanoxyuris belongs to the Oxyuridae family. The Trypanoxyuris sp. was identified by its oval, thickshelled, embryonated eggs. The eggs were 48–50 lm (n = 21, average = 49.0 lm, SD = 0.68) long and 23–27.5 lm (n = 21, average = 25.4 lm, SD = 1.55) wide (Fig. 1b).
Parasites detected in the fecal samples
Order Strongylida
We identified the presence of three helminth important to note that it was not possible to tozoa because preservation in formalin can morphology, so determinations would not be
species. It is identify proalter sample precise.
Controrchis sp. This trematode was identified by the presence of an ovalshaped dark red-brown egg with an operculum and a thick, well-defined outer shell. Individual lengths were 42.5–47.5 lm (n = 20, average = 45.2 lm, SD = 1.7)
Fig. 1 Parasitic forms observed. a Egg of Controrchis sp. (409); the germinal masses (MG) and the border of the operculum (Op) are visible. b Egg of Trypanoxyuris sp. (409), which is oval-shaped with a thick shell. Strongyloides sp. (409); this parasite was identified by the presence of c larvae with a rhabditiform esophagus (ER) and d embryonated eggs with a thin shell
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This parasite was identified as belonging to the order Rhabditida by the presence of embryonated eggs 54–57 lm long (n = 22, average = 55.7 lm, SD = 0.95) and 35.7–40 lm wide (n = 22, average = 38.1 lm, SD = 1.6) that were covered by a thin and transparent membrane. These egg characteristics indicated a nematode associated with the presence of a rhabditiform larval type. The first-stage larva of Strongyloides (rhabditiform larva) is usually the only parasitic nematode larva found in fresh fecal samples (Ash and Orihel 1997). Therefore, the characteristics of the egg (size and shape) and those of the larva (rhabditiform esophagus)
Parasites species richness Host species related All endoparasite species were found in the fecal samples of A. palliata and A. geoffroyi. Age related The three parasites were present in samples from adult and juvenile monkeys. Sex related Samples from males and females contained the three parasites. FRE Lactating and nonlactating females of both monkey species were infected with the three endoparasite species. Season related Samples taken during the dry and wet seasons from both monkey species contained the three endoparasite species. Prevalence of infection The prevalence of infection in A. palliata was 84 %, since 79 of the 94 individuals sampled presented at least one endoparasite species. In A. geoffroyi 100 % of the individuals presented at least one parasite species. The pattern of endoparasite prevalence depended on the parasite type and the primate species considered. When we compared parasite prevalence between the two monkey species, we found significant differences in Controrchis sp. (Fig. 2). The logistic analysis showed a higher prevalence of Controrchis sp. in A. palliata (v2 = 49.3; df = 1; P \ 0. 0001), while the prevalences of both Trypanoxyuris sp. (v2 = 9.2; df = 1; P = 0.9) and Strongyloides sp. (v2 = 14.1; df = 1; P = 0.9) was similar in the monkey species. Season related No significant differences were found in endoparasite prevalence between seasons in either species of monkey (Trypanoxyuris sp. v2 = 0.75; df = 1; P = 0.9; Controrchis sp. v2 = 1.11; df = 1; P = 0.9; Strongyloides sp. v2 = 7.2; df = 1; P = 0.8). The interaction between host species and season was not significant (Trypanoxyuris sp. v2 = 0.7; df = 1; P = 0.9; Controrchis sp. v2 = 0.1; df = 1; P = 0.8; Strongyloides sp. v2 = 12.2; df = 1; P = 0.9). Month nested in season also showed no differences (Trypanoxyuris sp. v2 = 4.37; df = 11; P = 0.9; Controrchis sp. v2 = 5.2; df = 11; P = 0.9; Strongyloides sp. v2 = 12.7; df = 11; P = 0.7). Coinfection We found differences in the patterns of infection by one, two, or three parasite species between the primate species. In A. palliata, some individuals were not infected (16 %), 33 % were infected with one parasite species, 45 % with two parasite species, while only 6 % were infected with three parasite species. In contrast, all individuals of A. geoffroyi were parasitized; among these,
Unparasitized One parasite species Two parasite species Three parasite species
70 60 50 40 30 20 10 0
A. palliata
A. geoffroyi
Fig. 2 Percentages of individuals of Alouatta palliata and Ateles geoffroyi infected by different numbers of parasite species. Binomial errors are show by the bars 80
Parasite prevalence (%)
indicate that the nematode belongs to the family Strongylidae (Fig. 1c, d).
Infected individuals (%)
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70
*
Alouatta palliata
Ateles geoffroyi
60 50 40 30 20 10 0 Controrchis sp.
Trypanoxyuris sp.
Strongyloides sp.
Species
Fig. 3 Comparison of the prevalence of each endoparasite species in Alouatta palliata and Ateles geoffroyi. Binomial errors are shown by the bars. Asterisk indicates a significant difference
62 % were infected with one parasite species, 35 % with two, and only 3 % with three parasite species (see Fig. 2). In addition, we found that all combinations of multiple parasite infections (2 or 3) were more likely than expected based on parasite prevalence alone (Controrchis sp.– Strongyloides sp., P = 0.0008; Controrchis sp.–Trypanoxyuris sp., P = 0.0001; Trypanoxyuris sp.–Strongyloides sp., P = 0.0015; Controrchis sp.–Trypanoxyuris sp.– Strongyloides sp., P = 0.00000001) (Fig. 3). Host age Adults and juveniles of both monkey species showed similar endoparasite prevalences (A. palliata: Trypanoxyuris sp. v2 = 0.4; df = 1; P = 0.8; Controrchis sp. v2 = 0.8; df = 1; P = 0.4; Strongyloides sp. v2 = 0.8; df = 1; P = 0.4. A. geoffroyi: Trypanoxyuris sp. v2 = 2.3; df = 1; P = 0.3; Controrchis sp. v2 = 0.12; df = 1; P = 0.09; Strongyloides sp. v2 = 0.9; df = 1; P = 0.9). Sex related We found that a higher proportion of males were infected with Trypanoxyuris sp. and Controrchis sp. than females (Table 1). FRE Lactating females showed a higher prevalence of infection with Controrchis sp. than nonlactating females (Table 1).
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Primates Table 1 Endoparasite prevalence in relation to host sex and female reproductive condition (FRE)
Controrchis sp. Prevalence %
Strongyloides sp. v
2
P \ Prevalence %
Trypanoxyuris sp. 2
v
P \ Prevalence %
v2
P\
0.3
0.6
Female 9.8 (0.02)
10.1
0.001
4.2
0.1
Nonlactating 12 (0.06)
A. palliata Sex
Female 68.6 (0.06)
FRE
Nonlactating 4 (0.04)
4.3
0.03
Female 43 (0.07)
6.7
0.03
Nonlactating 36 (0.09)
Male 92 (0.05)
Male 51 (0.1)
Lactating 65.3 (0.09)
Male 44 (0.1)
Lactating 42 (0.09)
1.5
0.5
0.1
0.9
2.2
0.3
Lactating 3.8 (0.03)
A. geoffroyi Binomial errors are shown in parentheses. The number of degrees of freedom is 1 in all cases Significant differences are shown in bold
Sex
Female 6.6 (0.04)
FRE
Juvenile 10 (0.1)
0.2
0.9
1.9
0.09
Male 10 (0.09)
0.1
0.9
0.9
0.09
Male 40 (0.15)
Adults 8 (0.5)
Discussion Our results show that the sympatric populations of A. palliata and A. geoffroyi had the same parasite species richness. We also found that infections by multiple parasite species (two or three) were more frequent than expected based on their prevalence alone in both monkey species, suggesting that coinfection by different parasite species is a common event in these sympatric primate populations. Some authors have suggested that multiple infections could be associated with high morbidity and mortality (Gillespie et al. 2005), and that multiple infections could be an important measure of environmental health (Chapman et al. 2006; Trejo-Macı´as et al. 2007). The parasites identified in this study have already been reported in wild populations of A. palliata in Costa Rica. Stuart et al. (1990) found that 22 % of fecal samples from Alouatta palliata contained eggs of Trypanoxyuris sp., 32 % presented Controrchis biliophilus, and 14 % contained a nematode from the order Strongylida. The authors argue that this high parasite species richness and prevalence are due to the high howling monkey density at this study site. Trejo-Macı´as et al. (2007) reported six parasite species (trematode I, trematode II, Controrchis biliophilus, Trypanoxyuris sp., Parabronema sp., and Coccidia), and found that parasite prevalence was higher in fragmented habitats than in continuous and/or protected forests. Valdespino et al. (2010) found three parasite species (one unidentified species of Eimeriidae, Trypanoxyuris minutus, and Controrchis biliophilus). The prevalence of T. minutus and the infection density for all parasites differed between seasons, and the largest fragment consistently differed from the other fragments. For Ateles geoffroyi, most parasite studies have reported different Strongyloides species in
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Female 53.3 (0.09) Juvenile 60 (0.15) Adults 44 (0.1)
Female 1 (0.02) Male 10 (0.1) Juvenile 14 (0.7) Adults 25 (0.15)
individuals in captivity (Gual et al. 1990; Rodrı´guez 1995). Strongyloides cebus and Controrchis biliophilus were found in Costa Rica in wild populations (Stuart et al. 1998), and Trypanoxyuris sp. was reported in Costa Rica and Quintana Roo, Me´xico (Stuart et al. 1998; Bonilla-Moheno 2002). Few studies have analyzed parasite infections in sympatric species, despite the fact that some authors have suggested that the parasite analyses of Neotropical primates should also consider other species of monkeys that are either sympatric or have been sympatric in recent history (Stuart et al. 1998). A study performed in Costa Rica reported that the prevalence of Controrchis biliophilus and Strongyloides cebus was higher in Alouatta sp. than in the sympatric species Ateles sp. and Cebus sp. (Stuart et al. 1998). Therefore, primate species that occur in the same neighborhood, such as howler and spider monkeys, are susceptible to the same parasite species (Freeland 1983). Our results show similar patterns, since we found that sympatric species A. palliata and A. geoffroyi shared the same parasite species, but with a higher prevalence of Controrchis sp. in A. palliata. Ecological and physiological differences between sympatric species may result in differential exposure and response to parasitic infection (Milton 1981; Freeland 1983; Zuk and McKean 1996). Howler monkeys may show higher parasite richness and prevalence because their populations occur in large groups, so there is increased risk of transmission (Kuris et al. 1980; Moller et al. 1993; Altizer et al. 2003). In contrast, A. geoffroyi is generally found in low-density populations (but see Wallace et al. 1998) with large home ranges (Gonza´lez-Zamora et al. 2009; Chaves et al. 2011), resulting in individuals being less exposed to infection sources.
Primates
One physiological difference between monkey species is the variation observed in their digestive strategies (Freeland 1983). The physiology of the digestive system of spider monkeys seems to be designed for a diet mainly composed of easily digestible food, such as fleshly fruits (Milton 1981; Lambert 1998). Meanwhile, howlers are highly folivorous (Milton 1981; Crockett and Eisenberg 1987), which exposes them to differential parasite infective stages (Freeland 1983). Moreover, it has been proposed that leaf-eating primates, such as howler monkeys, may experience higher parasitic diversity because the large volumes of plant matter they ingest may expose them to infective-stage pathogens (Vitone et al. 2004). In primates, the risk of parasite infection may depend on the complexity of the parasite’s life cycle (e.g., the number of intermediate hosts) (Valdespino et al. 2010). For example, the life cycle of Controrchis sp. is still unknown (Stuart et al. 1998; Eckert et al. 2006), but it is known to have an indirect life cycle, with a snail as the first intermediate host and then an arthropod (ant or wasp) as the second, infective intermediate host. Therefore, it is likely that primates may become infected with Controrchis sp. through the accidental consumption of the secondary intermediate host (Stuart et al. 1998; Campillo et al. 1999; Kowalzik et al. 2010). Parasite acquisition by primates may thus depend on the feeding behavior of the primate and the abundance and activity of the second intermediate host (Stuart et al. 1998; Kowalzik et al. 2010). Trypanoxyuris sp. and Strongyloides both have direct life cycles. In particular, in the case of Trypanoxyuris sp., the adults live in the colon and produce oocysts that are expelled through the feces. The cycle completes when the next host ingests eggs from contaminated food or water (Felt and White 2005). In the same way, Strongyloides sp. has a direct cycle in which the infective stage is a larva that infects the host by penetrating its skin or through the accidental ingestion of larvae in food or water (Campillo et al. 1999). Trypanoxyuris sp. is infective almost immediately after being shed in the host’s feces, leading to anal–oral transmission (Valdespino et al. 2010). In constrast, Strongyloides sp. can survive and reproduce in a free-living state as well inside the body of the host; ground contact or the ingestion of water or food contaminated with feces are the principal sources of infection (Campillo et al. 1999). In this way, the arboreal lifestyle of A. palliata and A. geoffroyi limits contact with the ground, and confers protection against infections by parasites with direct life cycles, such as Strongyloides sp. (Stuart et al. 1990, 1998). Strongyloides sp. is one of the most common parasites in Old World primates (Gilbert 1994), which suggests that individuals get infected by ingesting contaminated vegetation or through contact with soil-containing infective larvae, especially under sleeping trees (Meade 1983).
Alouatta species defecate at specific sites—often small gaps or locations that are free of underlying vegetation, thus avoiding contact with fecal material that could contain infectious forms (Montilha et al. 2002). Importance of host sex, host age, and female reproductive stage on endoparasite infections Our results show that males of A. palliata were more likely to be parasitized by Trypanoxyuris sp. and Controrchis sp. than females, but no differences in parasite prevalence were found between the sexes in A. geoffroyi. Trejo-Macı´as et al. (2007) found a similar pattern, where the females of A. palliata and A. pigra presented lower rates of infection with C. biliophilus than the males. We also found a higher prevalence of Controrchis sp. in lactating females of A. palliata. Sex, age, and reproductive status alter the expression of sex steroid hormones (Lamason et al. 2006) that modulate host immunoresponse in animals (Klein 2004). Females are expected to show more effective resistance to some parasite infections than males (O’Sullivan and Donald 1970; Lamason et al. 2006; Stoner and Gonza´lez-Di Pierro 2006). Lactating or pregnant females release hormones during gestation and lactation that have a depressor effect on the immune system, although this seems to be less relevant than the effect of testosterone (Zuk and McKean 1996). In our study it is not clear why the prevalence of Strongyloides sp. in males is not higher than that in females. It is known that each parasite species has a different infection pattern, and identifying the determinants of infection from among the broad array of ecological and physiological factors that influence each parasitic infection is difficult because of the complex interactions involved (Nunn and Altizer 2006). Variation in the sex patterns observed in the two primate species suggests that other factors in addition to hormones, such as level of exposure to the infective stage of the parasite, social behavior, habitat quality, diet, difference in activities between sexes (Bundy 1988), and acquired immunity (Zuk and McKean 1996), may contribute to differences in rates of parasite infection among the sexes (Klein 2004). For example, it has also been suggested that there is differential exposure of monkey species to the infective stages of parasites with direct cycles due to differences in sexual behavior. For instance, howler males nuzzle and lick female genitalia and also taste urine (Crockett and Eisenberg 1987), exposing them to the infective stages of parasites with direct cycles, such as Trypanoxyuris sp. (Crockett and Eisenberg 1987). Another example is lactating females, which have higher protein and mineral requirements (Oates 1986) and, in the case of A. palliata, lacting females show increased consumption of plants (Serio-Silva et al. 1999). This increases
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the possibility of exposure to infective stages that are in the vegetation, such as Controrchis sp. However, in our study, we did not analyze these aspects, so we cannot provide an accurate explanation for our results. Seasonal differences in endoparasitic infections Some studies of Allouata sp. and Ateles sp. have found that the presence of humid conditions increases the intensity and prevalence of endoparasitic infections (Stuart et al. 1990, 1993; Stoner 1996). In particular, some authors have found greater richness, intensity, and prevalence of parasitic infections during the rainy season than the dry season (Bonilla-Moheno 2002; Stoner and Gonza´lez-Di Pierro 2006; Trejo-Macı´as and Estrada 2012). However, our results do not support the hypothesis that intestinal parasitic infections of A. geoffroyi and A. palliata are higher in the rainy season than in the dry season. Similarly, some other studies have shown no seasonal variations in endoparasitic infections in primate populations (McGrew et al. 1989; Mu¨ller-Graf et al. 1997). It has been proposed that the prevalence and intensity of infection in dry forest may be lower than that in rainforest (Stoner 1996). In the tropical dry forests of Costa Rica, Stuart et al. (1998) found that A. palliata and A. geoffroyi had a total helminth prevalence of 48 and 16 %, respectively, while Stoner (1996) reported an endoparasite prevalence of 100 % in A. palliata living in a tropical rainforest. However, in our study, the total endoparasite prevalence was 84 % in A. palliata and 100 % in A. geoffroyi. Chinchilla et al. (2005) also found similar results for parasite prevalence in fecal samples of A. palliata in wet and dry forests. The authors suggested that parasitic infection of A. palliata is not dependent on humidity. It is important to mention that our study site is a forest fragment undergoing regeneration, with some areas of preserved forest and abandoned grassland. Forest fragmentation affects host–parasite interactions, increasing the intensity and prevalence of parasitic infection in natural communities due to changes in biotic and abiotic conditions (Gilbert 1994; Gillespie and Chapman 2008; PereaRodriguez et al. 2010). Although we did not compare forest fragments with continuous forest, our results could be influenced by the fragmentation process. We conclude from our study that A. palliata shows greater variation in patterns of endoparasitic infection than A. geoffroyi. Controrchis sp. was the parasite species that showed the greatest differences in prevalence between the monkey species, between the host sexes, and according to the female’s reproductive state. Since Controrchis sp. is acquired by the oral ingestion of a secondary intermediate host (ant or wasp), differences in the patterns of infection between A. palliata and A. geoffroyi, between the sexes, and
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between the reproductive states of females of A. palliata may be explained by differences in habitat use (diet, foraging behavior). In males and lactating females, the particular physiological conditions resulting from hormone regulation provide favorable internal conditions for parasites, determining the infection pattern. Thus, as stated by Stuart et al. (1998), Controchis sp. is likely the most useful parasite species for providing clues about the ecology and behavior of different primate species. Therefore, it is necessary to determine the life cycle of Controrchis sp. to understand its host behavior and habitat preferences. Because of the endangered status of Neotropical primates, it is imperative to understand the patterns of parasitic infection of such primates and the factors that determine them. The principal factors that influence endoparasite prevalence in howler and spider monkeys cannot be determined with precision until the life histories and transmission patterns of many parasites are known. In our study, season did not have a notable effect on endoparasite prevalence in either monkey species. We argue that it is necessary to examine more than one slide per specimen to obtain a better estimate of parasite species richness in primate populations. Finally, our study represents an important contribution to the study of parasite infections in monkey populations. We report a study of endoparasite species richness and prevalence in a wild population of Ateles geoffroyi, when most of the published studies on the parasites of this species focus on individuals in captivity (Gual et al. 1990; Rodrı´guez 1995). There are also few analyses of parasite patterns in sympatric monkey populations (Stuart et al. 1998), as well as in lactating female monkeys (Stoner 1996; Stoner and Gonza´lez-Di Pierro 2006), despite the fact that the parasite infection patterns of animals are known to be influenced by sex steroid hormones (Lamason et al. 2006). Acknowledgments We thank the authorities of the Guanacaste Conservation Area for their permission to conduct this study. This study was partially supported by a scholarship granted by CONACYT and UNAM.
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ORIGINAL ARTICLE
Patterns of infection by intestinal parasites in sympatric howler monkey (Alouatta palliata) and spider monkey (Ateles geoffroyi) populations in a tropical dry forest in Costa Rica Selene Maldonado-Lo´pez • Yurixhi Maldonado-Lo´pez Alberto Go´mez-Tagle Ch. • Pablo Cuevas-Reyes • Kathryn E. Stoner
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Received: 18 April 2013 / Accepted: 2 February 2014 Ó Japan Monkey Centre and Springer Japan 2014
Abstract In primate populations, endoparasite species richness and prevalence are associated with host traits such as reproductive and social status, age, sex, host population density, and environmental factors such as humidity. We analyzed the species richness and prevalence of intestinal parasites in two sympatric primate populations, one of Alouatta palliata and one of Ateles geoffroyi, found in a tropical dry forest in Costa Rica. We identified three species of intestinal parasites (Controrchis sp., Trypanoxyuris sp., and Strongyloides sp.) in these two primate species. We did not find any differences in species richness between the primate species. However, the prevalences of Controrchis sp. and Trypanoxyuris sp. were higher in Alouatta palliata. Similarly, males and lactating females of Alouatta palliata showed higher Controrchis sp. prevalences. We did not observe any differences in parasite richness and prevalence between seasons. Infectious diseases in endangered primate
S. Maldonado-Lo´pez (&) Y. Maldonado-Lo´pez Centro de Investigaciones en Ecosistemas, UNAM, Antigua Carretera a Pa´tzcuaro No. 8701, Col. Ex-Hacienda de San Jose´ de la Huerta, 58190 Morelia, Michoaca´n, Mexico e-mail: [email protected] A. Go´mez-Tagle Ch. INIRENA, Universidad Michoacana de San Nicola´s de Hidalgo, Ciudad Universitaria, 58030 Morelia, Michoaca´n, Mexico P. Cuevas-Reyes Laboratorio de Ecologı´a de Interacciones Bio´ticas, Facultad de Biologı´a, Universidad Michoacana de San Nicola´s de Hidalgo, Ciudad Universitaria, 58030 Morelia, Michoaca´n, Mexico K. E. Stoner Department of Fish, Wildlife and Conservation Ecology, New Mexico State University, MSC 4901, P.O. Box 30003, Las Cruces 88011, New Mexico, USA
populations must be considered in conservation strategies, especially when defining protected areas. Keywords Alouatta palliata Ateles geoffroyi Host sex Host age Endoparasites Tropical dry forest
Introduction Endoparasitic infections are very common in nonhuman primate populations (Stuart et al. 1990, 1998; Stoner 1996; Altizer et al. 2003; Nunn et al. 2003; Stoner and Gonza´lezDi Pierro 2006; Gillespie and Chapman 2008; Valdespino et al. 2010). Many of these parasites act as commensals most of the time, but they are pathogenic when the resistance of the host is depressed or their abundance is unusually high (Amato et al. 2002; Chapman et al. 2006; Martı´nez-Mota et al. 2007). The high species richness and prevalence of endoparasites in wild primate populations are associated with some host traits such as reproductive and social status, age, sex, and host population density (Altizer et al. 2003; Godoy et al. 2004; Eckert et al. 2006; Trejo-Macı´as et al. 2007; Raharivololona and Ganzhorn 2009; Pebsworth et al. 2012; Trejo-Macı´as and Estrada 2012; Vitazkova and Wade 2007). For example, primates that show highly social behavior are more exposed to infective stages of endoparasites (Gilbert 1994). In high-density primate populations, high endoparasite species richness and prevalence might be expected, because the chance that a primate in such a population will be found by endoparasites is greater than the chance that they will be found as an isolated primate. In this case, a response by the endoparasites to the amount of resources available is implied, with host proximity regulating endoparasite population size via density-
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dependent mechanisms (Freeland 1980; Stuart et al. 1990; Altizer et al. 2003; Nunn et al. 2003; Valdespino et al. 2010). In primate species that occur in sympatric conditions, both populations are susceptible to the same parasite species as a result of the proximity of the primates in the neighborhood (Freeland 1983; Stuart et al. 1998). Sex, age, and reproductive status affect the expression of sex steroid hormones (i.e., estrogen, progesterone, and testosterone) (Lamason et al. 2006) that modulate host immunoresponse in animals (Klein 2004). Estrogen stimulates the immune system, while progesterone and testosterone are considered immunosuppressors (Klein 2004; Trejo-Macı´as et al. 2007). Therefore, females might be expected to offer more effective resistance against some parasitic infections than males. However, lactating or pregnant females (O’Sullivan and Donald 1970; Lamason et al. 2006; Stoner and Gonza´lez-Di Pierro 2006), as well as primates with secondary reproductive character development (juvenile stages), have lower resistance to parasitic infections (Lamason et al. 2006; Mu¨ller-Graf et al. 1997; Stoner and Gonza´lez-Di Pierro 2006). In the same way, environmental factors such as humidity can promote the survival, development, and transmission of the infective stages of endoparasites (Stuart et al. 1990, 1993; Jones 1994; Stoner 1996, Bonilla-Moheno 2002; Eckert et al. 2006). Therefore, primates living in humid environments may show higher endoparasite species richness and prevalence (Stuart et al. 1990, 1993; Jones 1994; Stoner 1996, 1996; Stuart et al. 1998; Stoner and Gonza´lez-Di Pierro 2006; Cristo´bal-Azkarate et al. 2010; Valdespino et al. 2010; Trejo-Macı´as and Estrada 2012). It is particularly important to identify the factors that affect parasitic infections in wild primate populations (Gilbert 1994; Stoner 1996; Stuart et al. 1998; Gillespie and Chapman 2008), especially endangered primate species such as Alouatta palliata and Ateles geoffroyi (UICN 2002), which have been displaced to fragmented forests and disturbed areas (Arroyo-Rodrı´guez and Dias 2010; Chaves et al. 2011) in many regions in which they occur. Several studies have described endoparasitic infections of howler monkeys (Alouatta sp.) (Neville 1972; Stuart et al. 1990, 1998; Gilbert 1994; Stoner 1996; Stoner and Gonza´lez-Di Pierro 2006; Valdespino et al. 2010; Trejo-Macı´as et al. 2007; Trejo-Macı´as and Estrada 2012) but only a few studies have documented endoparasitic infections in spider monkeys (Ateles sp.) in the wild (Bonilla-Moheno 2002). Similarly, little information exists about patterns of parasitic infection of sympatric primate species. Stuart et al. (1998) demonstrated differences among primate species in parasite prevalence, with 49 % of Ateles, 51 % of Alouatta, and 91 % of Cebus found to be parasitized. Furthermore, Controrchis biliophilus prevalence was higher in Alouatta than in Ateles or Cebus species.
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In our study, we analyzed and compared the richness and prevalence of the endoparasites in two sympatric monkey populations—one of Alouatta palliata and one of Ateles geoffroyi—inhabiting a tropical dry forest fragment with strong seasonality. We hypothesized that Alouatta palliata and Ateles geoffroyi share the same intestinal parasite species since they are sympatric species that occupy the same home range in the study site (Freeland 1983). However, we expected different percentages of parasitic infection (prevalence) for the two primate species as a result of their intrinsic physiological and ecological differences (Milton 1981; Freeland 1983). Our objectives were (1) to analyze and compare differences in endoparasite richness and prevalence between sympatric populations of A. palliata and A. geoffroyi; (2) to evaluate the importance of host sex, host age, and female reproductive stage (FRE) in endoparasite infections of A. palliata and A. geoffroyi populations; and (3) to analyze the effects of seasonality on endoparasite infection.
Methods Study area This study was conducted in the Tropical Dry Forest of Santa Rosa National Park in Costa Rica, in the Murcie´lago section, Guanacaste Conservation Area, situated in northwestern Costa Rica. This area was declared part of the Santa Rosa National Park in 1980 (Janzen 1986); it is a mountainous area covering approximately 122 km2 with low hills and forests. It is a seasonal forest with a severe dry season from December to May and an annual rainfall of 900–2500 mm (Janzen 1986; Hiramatsu et al. 2008). As a result of livestock, deforestation, and agriculture, the Murcie´lago section currently presents a mosaic of vegetation that includes secondary forests, abandoned pastures, and forest fragments. The populations of Alouatta palliata and Ateles geoffroyi studied occur in sympatry in a forest fragment with deciduous and riparian vegetation. Study species Alouatta palliata This is the only genus of the subfamily Alouattinae of the neotropical family Cebidae (Napier 1976). The genus Alouatta includes six species that are distributed from southern Mexico to northern Argentina (Wolfheim 1983; Crockett and Eisenberg 1987). In particular, A. palliata is found from southern Mexico, possibly southern Guatemala, and from Honduras through Central America to Colombia and western Ecuador (Crockett and Eisenberg 1987). The
Primates
howler monkey has the widest distribution of all the Neotropical primates, and occupies a vast range of habitat types (Crockett and Eisenberg 1987). It is found at elevations of 2,300 m in moist evergreen habitats and in semideciduous habitats with marked seasonality (Mittermeier and van Roosmalen 1981; Crockett and Eisenberg 1987). Alouatta palliata is the largest of the Neotropical primates, with adults weighing from 4 to 10 kg, and it has clear sexual dimorphism, as males can be more than twice as heavy as females. Howler monkeys are primarily folivores, although they can consume a considerable amount of fruit depending on the location or time of year (Reid 1997). Ateles geoffroyi This species has nine subspecies that are separated almost entirely on the basis of fur color (Kellogg and Goldman 1944). The spider monkey is distributed over a vast area in Central America and South America. It is located from the southern River Yapacani in Bolivia to northern Mexico in the eastern coastal state of Tamaulipas. Ateles geoffroyi in central America seems to be more flexible in its habitat selection than most of its South American relatives. In Costa Rica, it has been observed in evergreen, semideciduous, and deciduous forests (Freese 1976). The genus Ateles is primarily frugivorous, selecting the soft parts of a great variety of fruits. Other parts of the plants, such as young leaves, flowers, and bark, are less commonly consumed by the spider monkey (Reid 1997; Di Fiore et al. 2008). They can also passively eat some insects such as larvae and wasps that are usually found in the plant species they consume (van Roosmalen and Klein 1988). Fecal sampling, preservation, and analysis Alouatta palliata and Ateles geoffroyi are threatened species (UICN 2002), and it was necessary to identify endoparasites using a noninvasive procedure that provides data on the richness and prevalence of parasitic infections (Gillespie 2006). Samples from two sympatric troops of primates, one of A. palliata and the other of A. geoffroyi, were collected between May 2000 and March 2001, and included data collected during both the wet (June– November) and dry (December–May) seasons. Troops were followed, and samples were collected at the time of defecation during the morning. Using a spatula, we carefully collected the top and central parts of the fecal sample to avoid contact with the ground and contamination with other organisms. Fresh feces from individual monkeys were stored immediately after defecation in sterile vials with 10 % formalin. The same quantity was collected for each sample by adding feces until the formalin was displaced a given amount. We recorded the date, time of
collection, and identity of the individual observed (name, sex, age, FRE). In total, we collected fecal samples from 134 individuals: 94 samples of A. palliata and 40 of A. geoffroyi. Parasites were identified by the presence of eggs and larvae in the feces. To determine the species richness of endoparasites and their prevalence in the hosts, we performed two different analyses (i.e., qualitative and quantitative). In the qualitative analysis, the presence of eggs and larvae were determined by direct microscopic observation of the samples. For each sample we prepared two slides, and in each one we deposited two sample drops and one drop of Lugol’s iodine solution under a coverslip (24 9 50 mm). We systematically observed the entire slide under 209 and 409 objectives and taxonomically identified each endoparasite species. In the quantitative analysis, the number of eggs and larvae was determined after sample sedimentation using a formalin-ethyl acetate centrifugation technique (Long et al. 1985). After centrifugation, two drops of the prepared sample and one drop of Lugol’s iodine solution were placed on a microscope slide with a glass coverslip (24 9 50 mm). Four slides of each sample were examined systematically with a compound microscope. Parasites were identified on the basis of egg and larvae morphology and size, measured at 4009 to the nearest 0.1 lm with an ocular micrometer. Most studies that have evaluated parasite–primate interactions have assumed that parasite species richness can be estimated using a single slide per sample (Stuart et al. 1990). However, in a preliminary analysis, we found that parasite species richness is underestimated when it is analyzed using a single slide per sample rather than four slides per sample, indicating that parasite richness can vary significantly in accord with the number of slides analyzed in the study. Therefore, we decided to examine four slides per sample in our study. Statistical analysis In order to determine the differences in infection prevalence between the monkey species and between seasons, we conducted a single logistic regression analysis using the GENMOD procedure (SAS 2000). The analysis incorporated host species, month nested in season, and the interaction between host species and season as independent variables and the percentage of infected individuals as the response variable. In the analysis we used a binomial distribution (presence–absence) and a logit link function. To determine if some combinations of parasite species (co-infections per pair of parasite species) are more or less likely to occur than expected from their prevalence alone in the host primate species, we used Fisher’s exact test.
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Primates
To analyze the differences in parasite prevalence between host sex, host age, and FRE in A. paliatta and A. geoffroyi, we performed a logistic regression analysis using the GENMOD procedure (SAS 2000) for each parasite species. The model used host sex, host age, and FRE as independent categorical variables and the percentage of infected individuals as the dependent variable. In the analysis, we used a binomial distribution and a logit link function.
and their widths were 20–22.5 lm (n = 20, average = 21.4 lm, SD = 0.83). The germinal masses were visible below the operculum in most of them (Fig. 1a). Trypanoxyuris sp.
Results
The genus Trypanoxyuris belongs to the Oxyuridae family. The Trypanoxyuris sp. was identified by its oval, thickshelled, embryonated eggs. The eggs were 48–50 lm (n = 21, average = 49.0 lm, SD = 0.68) long and 23–27.5 lm (n = 21, average = 25.4 lm, SD = 1.55) wide (Fig. 1b).
Parasites detected in the fecal samples
Order Strongylida
We identified the presence of three helminth important to note that it was not possible to tozoa because preservation in formalin can morphology, so determinations would not be
species. It is identify proalter sample precise.
Controrchis sp. This trematode was identified by the presence of an ovalshaped dark red-brown egg with an operculum and a thick, well-defined outer shell. Individual lengths were 42.5–47.5 lm (n = 20, average = 45.2 lm, SD = 1.7)
Fig. 1 Parasitic forms observed. a Egg of Controrchis sp. (409); the germinal masses (MG) and the border of the operculum (Op) are visible. b Egg of Trypanoxyuris sp. (409), which is oval-shaped with a thick shell. Strongyloides sp. (409); this parasite was identified by the presence of c larvae with a rhabditiform esophagus (ER) and d embryonated eggs with a thin shell
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This parasite was identified as belonging to the order Rhabditida by the presence of embryonated eggs 54–57 lm long (n = 22, average = 55.7 lm, SD = 0.95) and 35.7–40 lm wide (n = 22, average = 38.1 lm, SD = 1.6) that were covered by a thin and transparent membrane. These egg characteristics indicated a nematode associated with the presence of a rhabditiform larval type. The first-stage larva of Strongyloides (rhabditiform larva) is usually the only parasitic nematode larva found in fresh fecal samples (Ash and Orihel 1997). Therefore, the characteristics of the egg (size and shape) and those of the larva (rhabditiform esophagus)
Parasites species richness Host species related All endoparasite species were found in the fecal samples of A. palliata and A. geoffroyi. Age related The three parasites were present in samples from adult and juvenile monkeys. Sex related Samples from males and females contained the three parasites. FRE Lactating and nonlactating females of both monkey species were infected with the three endoparasite species. Season related Samples taken during the dry and wet seasons from both monkey species contained the three endoparasite species. Prevalence of infection The prevalence of infection in A. palliata was 84 %, since 79 of the 94 individuals sampled presented at least one endoparasite species. In A. geoffroyi 100 % of the individuals presented at least one parasite species. The pattern of endoparasite prevalence depended on the parasite type and the primate species considered. When we compared parasite prevalence between the two monkey species, we found significant differences in Controrchis sp. (Fig. 2). The logistic analysis showed a higher prevalence of Controrchis sp. in A. palliata (v2 = 49.3; df = 1; P \ 0. 0001), while the prevalences of both Trypanoxyuris sp. (v2 = 9.2; df = 1; P = 0.9) and Strongyloides sp. (v2 = 14.1; df = 1; P = 0.9) was similar in the monkey species. Season related No significant differences were found in endoparasite prevalence between seasons in either species of monkey (Trypanoxyuris sp. v2 = 0.75; df = 1; P = 0.9; Controrchis sp. v2 = 1.11; df = 1; P = 0.9; Strongyloides sp. v2 = 7.2; df = 1; P = 0.8). The interaction between host species and season was not significant (Trypanoxyuris sp. v2 = 0.7; df = 1; P = 0.9; Controrchis sp. v2 = 0.1; df = 1; P = 0.8; Strongyloides sp. v2 = 12.2; df = 1; P = 0.9). Month nested in season also showed no differences (Trypanoxyuris sp. v2 = 4.37; df = 11; P = 0.9; Controrchis sp. v2 = 5.2; df = 11; P = 0.9; Strongyloides sp. v2 = 12.7; df = 11; P = 0.7). Coinfection We found differences in the patterns of infection by one, two, or three parasite species between the primate species. In A. palliata, some individuals were not infected (16 %), 33 % were infected with one parasite species, 45 % with two parasite species, while only 6 % were infected with three parasite species. In contrast, all individuals of A. geoffroyi were parasitized; among these,
Unparasitized One parasite species Two parasite species Three parasite species
70 60 50 40 30 20 10 0
A. palliata
A. geoffroyi
Fig. 2 Percentages of individuals of Alouatta palliata and Ateles geoffroyi infected by different numbers of parasite species. Binomial errors are show by the bars 80
Parasite prevalence (%)
indicate that the nematode belongs to the family Strongylidae (Fig. 1c, d).
Infected individuals (%)
Primates
70
*
Alouatta palliata
Ateles geoffroyi
60 50 40 30 20 10 0 Controrchis sp.
Trypanoxyuris sp.
Strongyloides sp.
Species
Fig. 3 Comparison of the prevalence of each endoparasite species in Alouatta palliata and Ateles geoffroyi. Binomial errors are shown by the bars. Asterisk indicates a significant difference
62 % were infected with one parasite species, 35 % with two, and only 3 % with three parasite species (see Fig. 2). In addition, we found that all combinations of multiple parasite infections (2 or 3) were more likely than expected based on parasite prevalence alone (Controrchis sp.– Strongyloides sp., P = 0.0008; Controrchis sp.–Trypanoxyuris sp., P = 0.0001; Trypanoxyuris sp.–Strongyloides sp., P = 0.0015; Controrchis sp.–Trypanoxyuris sp.– Strongyloides sp., P = 0.00000001) (Fig. 3). Host age Adults and juveniles of both monkey species showed similar endoparasite prevalences (A. palliata: Trypanoxyuris sp. v2 = 0.4; df = 1; P = 0.8; Controrchis sp. v2 = 0.8; df = 1; P = 0.4; Strongyloides sp. v2 = 0.8; df = 1; P = 0.4. A. geoffroyi: Trypanoxyuris sp. v2 = 2.3; df = 1; P = 0.3; Controrchis sp. v2 = 0.12; df = 1; P = 0.09; Strongyloides sp. v2 = 0.9; df = 1; P = 0.9). Sex related We found that a higher proportion of males were infected with Trypanoxyuris sp. and Controrchis sp. than females (Table 1). FRE Lactating females showed a higher prevalence of infection with Controrchis sp. than nonlactating females (Table 1).
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Primates Table 1 Endoparasite prevalence in relation to host sex and female reproductive condition (FRE)
Controrchis sp. Prevalence %
Strongyloides sp. v
2
P \ Prevalence %
Trypanoxyuris sp. 2
v
P \ Prevalence %
v2
P\
0.3
0.6
Female 9.8 (0.02)
10.1
0.001
4.2
0.1
Nonlactating 12 (0.06)
A. palliata Sex
Female 68.6 (0.06)
FRE
Nonlactating 4 (0.04)
4.3
0.03
Female 43 (0.07)
6.7
0.03
Nonlactating 36 (0.09)
Male 92 (0.05)
Male 51 (0.1)
Lactating 65.3 (0.09)
Male 44 (0.1)
Lactating 42 (0.09)
1.5
0.5
0.1
0.9
2.2
0.3
Lactating 3.8 (0.03)
A. geoffroyi Binomial errors are shown in parentheses. The number of degrees of freedom is 1 in all cases Significant differences are shown in bold
Sex
Female 6.6 (0.04)
FRE
Juvenile 10 (0.1)
0.2
0.9
1.9
0.09
Male 10 (0.09)
0.1
0.9
0.9
0.09
Male 40 (0.15)
Adults 8 (0.5)
Discussion Our results show that the sympatric populations of A. palliata and A. geoffroyi had the same parasite species richness. We also found that infections by multiple parasite species (two or three) were more frequent than expected based on their prevalence alone in both monkey species, suggesting that coinfection by different parasite species is a common event in these sympatric primate populations. Some authors have suggested that multiple infections could be associated with high morbidity and mortality (Gillespie et al. 2005), and that multiple infections could be an important measure of environmental health (Chapman et al. 2006; Trejo-Macı´as et al. 2007). The parasites identified in this study have already been reported in wild populations of A. palliata in Costa Rica. Stuart et al. (1990) found that 22 % of fecal samples from Alouatta palliata contained eggs of Trypanoxyuris sp., 32 % presented Controrchis biliophilus, and 14 % contained a nematode from the order Strongylida. The authors argue that this high parasite species richness and prevalence are due to the high howling monkey density at this study site. Trejo-Macı´as et al. (2007) reported six parasite species (trematode I, trematode II, Controrchis biliophilus, Trypanoxyuris sp., Parabronema sp., and Coccidia), and found that parasite prevalence was higher in fragmented habitats than in continuous and/or protected forests. Valdespino et al. (2010) found three parasite species (one unidentified species of Eimeriidae, Trypanoxyuris minutus, and Controrchis biliophilus). The prevalence of T. minutus and the infection density for all parasites differed between seasons, and the largest fragment consistently differed from the other fragments. For Ateles geoffroyi, most parasite studies have reported different Strongyloides species in
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Female 53.3 (0.09) Juvenile 60 (0.15) Adults 44 (0.1)
Female 1 (0.02) Male 10 (0.1) Juvenile 14 (0.7) Adults 25 (0.15)
individuals in captivity (Gual et al. 1990; Rodrı´guez 1995). Strongyloides cebus and Controrchis biliophilus were found in Costa Rica in wild populations (Stuart et al. 1998), and Trypanoxyuris sp. was reported in Costa Rica and Quintana Roo, Me´xico (Stuart et al. 1998; Bonilla-Moheno 2002). Few studies have analyzed parasite infections in sympatric species, despite the fact that some authors have suggested that the parasite analyses of Neotropical primates should also consider other species of monkeys that are either sympatric or have been sympatric in recent history (Stuart et al. 1998). A study performed in Costa Rica reported that the prevalence of Controrchis biliophilus and Strongyloides cebus was higher in Alouatta sp. than in the sympatric species Ateles sp. and Cebus sp. (Stuart et al. 1998). Therefore, primate species that occur in the same neighborhood, such as howler and spider monkeys, are susceptible to the same parasite species (Freeland 1983). Our results show similar patterns, since we found that sympatric species A. palliata and A. geoffroyi shared the same parasite species, but with a higher prevalence of Controrchis sp. in A. palliata. Ecological and physiological differences between sympatric species may result in differential exposure and response to parasitic infection (Milton 1981; Freeland 1983; Zuk and McKean 1996). Howler monkeys may show higher parasite richness and prevalence because their populations occur in large groups, so there is increased risk of transmission (Kuris et al. 1980; Moller et al. 1993; Altizer et al. 2003). In contrast, A. geoffroyi is generally found in low-density populations (but see Wallace et al. 1998) with large home ranges (Gonza´lez-Zamora et al. 2009; Chaves et al. 2011), resulting in individuals being less exposed to infection sources.
Primates
One physiological difference between monkey species is the variation observed in their digestive strategies (Freeland 1983). The physiology of the digestive system of spider monkeys seems to be designed for a diet mainly composed of easily digestible food, such as fleshly fruits (Milton 1981; Lambert 1998). Meanwhile, howlers are highly folivorous (Milton 1981; Crockett and Eisenberg 1987), which exposes them to differential parasite infective stages (Freeland 1983). Moreover, it has been proposed that leaf-eating primates, such as howler monkeys, may experience higher parasitic diversity because the large volumes of plant matter they ingest may expose them to infective-stage pathogens (Vitone et al. 2004). In primates, the risk of parasite infection may depend on the complexity of the parasite’s life cycle (e.g., the number of intermediate hosts) (Valdespino et al. 2010). For example, the life cycle of Controrchis sp. is still unknown (Stuart et al. 1998; Eckert et al. 2006), but it is known to have an indirect life cycle, with a snail as the first intermediate host and then an arthropod (ant or wasp) as the second, infective intermediate host. Therefore, it is likely that primates may become infected with Controrchis sp. through the accidental consumption of the secondary intermediate host (Stuart et al. 1998; Campillo et al. 1999; Kowalzik et al. 2010). Parasite acquisition by primates may thus depend on the feeding behavior of the primate and the abundance and activity of the second intermediate host (Stuart et al. 1998; Kowalzik et al. 2010). Trypanoxyuris sp. and Strongyloides both have direct life cycles. In particular, in the case of Trypanoxyuris sp., the adults live in the colon and produce oocysts that are expelled through the feces. The cycle completes when the next host ingests eggs from contaminated food or water (Felt and White 2005). In the same way, Strongyloides sp. has a direct cycle in which the infective stage is a larva that infects the host by penetrating its skin or through the accidental ingestion of larvae in food or water (Campillo et al. 1999). Trypanoxyuris sp. is infective almost immediately after being shed in the host’s feces, leading to anal–oral transmission (Valdespino et al. 2010). In constrast, Strongyloides sp. can survive and reproduce in a free-living state as well inside the body of the host; ground contact or the ingestion of water or food contaminated with feces are the principal sources of infection (Campillo et al. 1999). In this way, the arboreal lifestyle of A. palliata and A. geoffroyi limits contact with the ground, and confers protection against infections by parasites with direct life cycles, such as Strongyloides sp. (Stuart et al. 1990, 1998). Strongyloides sp. is one of the most common parasites in Old World primates (Gilbert 1994), which suggests that individuals get infected by ingesting contaminated vegetation or through contact with soil-containing infective larvae, especially under sleeping trees (Meade 1983).
Alouatta species defecate at specific sites—often small gaps or locations that are free of underlying vegetation, thus avoiding contact with fecal material that could contain infectious forms (Montilha et al. 2002). Importance of host sex, host age, and female reproductive stage on endoparasite infections Our results show that males of A. palliata were more likely to be parasitized by Trypanoxyuris sp. and Controrchis sp. than females, but no differences in parasite prevalence were found between the sexes in A. geoffroyi. Trejo-Macı´as et al. (2007) found a similar pattern, where the females of A. palliata and A. pigra presented lower rates of infection with C. biliophilus than the males. We also found a higher prevalence of Controrchis sp. in lactating females of A. palliata. Sex, age, and reproductive status alter the expression of sex steroid hormones (Lamason et al. 2006) that modulate host immunoresponse in animals (Klein 2004). Females are expected to show more effective resistance to some parasite infections than males (O’Sullivan and Donald 1970; Lamason et al. 2006; Stoner and Gonza´lez-Di Pierro 2006). Lactating or pregnant females release hormones during gestation and lactation that have a depressor effect on the immune system, although this seems to be less relevant than the effect of testosterone (Zuk and McKean 1996). In our study it is not clear why the prevalence of Strongyloides sp. in males is not higher than that in females. It is known that each parasite species has a different infection pattern, and identifying the determinants of infection from among the broad array of ecological and physiological factors that influence each parasitic infection is difficult because of the complex interactions involved (Nunn and Altizer 2006). Variation in the sex patterns observed in the two primate species suggests that other factors in addition to hormones, such as level of exposure to the infective stage of the parasite, social behavior, habitat quality, diet, difference in activities between sexes (Bundy 1988), and acquired immunity (Zuk and McKean 1996), may contribute to differences in rates of parasite infection among the sexes (Klein 2004). For example, it has also been suggested that there is differential exposure of monkey species to the infective stages of parasites with direct cycles due to differences in sexual behavior. For instance, howler males nuzzle and lick female genitalia and also taste urine (Crockett and Eisenberg 1987), exposing them to the infective stages of parasites with direct cycles, such as Trypanoxyuris sp. (Crockett and Eisenberg 1987). Another example is lactating females, which have higher protein and mineral requirements (Oates 1986) and, in the case of A. palliata, lacting females show increased consumption of plants (Serio-Silva et al. 1999). This increases
123
Primates
the possibility of exposure to infective stages that are in the vegetation, such as Controrchis sp. However, in our study, we did not analyze these aspects, so we cannot provide an accurate explanation for our results. Seasonal differences in endoparasitic infections Some studies of Allouata sp. and Ateles sp. have found that the presence of humid conditions increases the intensity and prevalence of endoparasitic infections (Stuart et al. 1990, 1993; Stoner 1996). In particular, some authors have found greater richness, intensity, and prevalence of parasitic infections during the rainy season than the dry season (Bonilla-Moheno 2002; Stoner and Gonza´lez-Di Pierro 2006; Trejo-Macı´as and Estrada 2012). However, our results do not support the hypothesis that intestinal parasitic infections of A. geoffroyi and A. palliata are higher in the rainy season than in the dry season. Similarly, some other studies have shown no seasonal variations in endoparasitic infections in primate populations (McGrew et al. 1989; Mu¨ller-Graf et al. 1997). It has been proposed that the prevalence and intensity of infection in dry forest may be lower than that in rainforest (Stoner 1996). In the tropical dry forests of Costa Rica, Stuart et al. (1998) found that A. palliata and A. geoffroyi had a total helminth prevalence of 48 and 16 %, respectively, while Stoner (1996) reported an endoparasite prevalence of 100 % in A. palliata living in a tropical rainforest. However, in our study, the total endoparasite prevalence was 84 % in A. palliata and 100 % in A. geoffroyi. Chinchilla et al. (2005) also found similar results for parasite prevalence in fecal samples of A. palliata in wet and dry forests. The authors suggested that parasitic infection of A. palliata is not dependent on humidity. It is important to mention that our study site is a forest fragment undergoing regeneration, with some areas of preserved forest and abandoned grassland. Forest fragmentation affects host–parasite interactions, increasing the intensity and prevalence of parasitic infection in natural communities due to changes in biotic and abiotic conditions (Gilbert 1994; Gillespie and Chapman 2008; PereaRodriguez et al. 2010). Although we did not compare forest fragments with continuous forest, our results could be influenced by the fragmentation process. We conclude from our study that A. palliata shows greater variation in patterns of endoparasitic infection than A. geoffroyi. Controrchis sp. was the parasite species that showed the greatest differences in prevalence between the monkey species, between the host sexes, and according to the female’s reproductive state. Since Controrchis sp. is acquired by the oral ingestion of a secondary intermediate host (ant or wasp), differences in the patterns of infection between A. palliata and A. geoffroyi, between the sexes, and
123
between the reproductive states of females of A. palliata may be explained by differences in habitat use (diet, foraging behavior). In males and lactating females, the particular physiological conditions resulting from hormone regulation provide favorable internal conditions for parasites, determining the infection pattern. Thus, as stated by Stuart et al. (1998), Controchis sp. is likely the most useful parasite species for providing clues about the ecology and behavior of different primate species. Therefore, it is necessary to determine the life cycle of Controrchis sp. to understand its host behavior and habitat preferences. Because of the endangered status of Neotropical primates, it is imperative to understand the patterns of parasitic infection of such primates and the factors that determine them. The principal factors that influence endoparasite prevalence in howler and spider monkeys cannot be determined with precision until the life histories and transmission patterns of many parasites are known. In our study, season did not have a notable effect on endoparasite prevalence in either monkey species. We argue that it is necessary to examine more than one slide per specimen to obtain a better estimate of parasite species richness in primate populations. Finally, our study represents an important contribution to the study of parasite infections in monkey populations. We report a study of endoparasite species richness and prevalence in a wild population of Ateles geoffroyi, when most of the published studies on the parasites of this species focus on individuals in captivity (Gual et al. 1990; Rodrı´guez 1995). There are also few analyses of parasite patterns in sympatric monkey populations (Stuart et al. 1998), as well as in lactating female monkeys (Stoner 1996; Stoner and Gonza´lez-Di Pierro 2006), despite the fact that the parasite infection patterns of animals are known to be influenced by sex steroid hormones (Lamason et al. 2006). Acknowledgments We thank the authorities of the Guanacaste Conservation Area for their permission to conduct this study. This study was partially supported by a scholarship granted by CONACYT and UNAM.
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