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Reproduction in free-ranging Propithecus verreauxi: estrus and the relationship between multiple partner matings and fertilization.

Female sifaka mate selectively with one or more resident and/or non-resident males during the breeding season. Various adaptive explanations have been advanced to explain why female primates mate with multiple males including that 1) females seek to confuse paternity and thereby forestall male infanticide and/or ensure male infant care or 2) females seek to ensure fertilization. Assessing the power of fertilization insurance to explain mating patterns in females requires information on the temporal relationship between mating and ovarian hormones. The hormonal correlates of reproduction and mating in free-ranging Propithecus verreauxi were investigated using excreted steroids as indices of reproductive state. Solid-phase extraction and radioimmunoassay techniques were used to measure unconjugated estradiol (E(2)) and progesterone (P(4)) in 485 desiccated fecal samples collected from five female sifaka before and during the breeding season at Beza Mahafaly, Madagascar. Results suggest that behavioral estrus was characterized by 10 to 15-day elevations in E(2); hormonal activity was observed to be similar to pseudo-estrus reported for other lemur species; apparent conception was associated with sustained P4 elevations beginning 1 to 3 days post-estrus with gestational phase elevations of E2 beginning 42 to 45 days post-conception; and mating with multiple partners appeared not to be a prerequisite to fertilization, as conception resulted from both monoandrous and polyandrous matings. These preliminary data suggest that fertilization insurance is not adequate to explain polyandrous mating in sifaka at Beza Mahafaly.

Animals↗

Recent advances in noninvasive techniques to monitor hormone-behavior interactions.

This paper reviews recent advances in field endocrinology, a focus as well as a method in primatology and behavioral ecology that permits the examination of social behavior and life history through hormonal investigations in natural settings. Endocrine data complements the traditional behavioral data collected by field scientists by providing quantitative measures for the examination of adaptive tradeoffs, costs of social strategies, and reproductive and social significance of mating events. Further, investigations of the physiological mechanisms of reproductive constraint provide tests of the adaptive significance of reproductive skew in cooperative and competitive breeders. Hormone data also can provide insights into the costs of competition and aggression and the role of temperament in individual reproductive success and the evolution of social systems. New, noninvasive methods for the collection of this information have augmented and expanded field endocrinology through the use of techniques that do not require potentially confounding physical or physiological manipulations. Specifically, urine and fecal samples can be collected from free-ranging animals and contain gonadal and adrenal hormones that parallel profiles of serum hormones. Sampling, preservation, extraction, and assay methods for the analysis of excreted steroids are reviewed along with the species and questions to which these methods have been applied.

Animals↗

Experimental African HEV infection in cynomolgus macaques (Macaca fascicularis).

Experimental infection with hepatitis E virus (HEV) from Africa has not been investigated. Our purpose was to study hepatitis E produced by HEV from Chad (North Africa) and to analyze the genetic sequence of the HEV obtained after animal passage. An HEV-containing fecal sample from Chad was intravenously inoculated in four cynomolgus macaques. When serum Alanine Amino Transferase (ALT) levels rose, open liver biopsy and bile aspiration were performed. In all the monkeys, an ALT rise occurred 25 to 32 days after inoculation and new anti-HEV was detected by Enzyme Immuno Assay (EIA). Hepatic histopathology was consistent with acute viral hepatitis. HEV was detected by polymerase chain reaction (PCR) in bile (3/4 animals) and feces (2/4 animals) and by imunoelectron microscopy (IEM) in the inoculum and one bile specimen. A genetic variant HEV was identified in one monkey. The Chad HEV produced hepatitis E with pathophysiologic and histopathologic findings similar to those observed with HEV from other geographic origins. A genomic variant HEV population was produced after one passage in a macaque.

Alanine Transaminase↗

Phylogenetic analysis of hepatitis E virus isolates from Egypt.

Hepatitis E virus (HEV) genome was detected by reverse transcriptase-polymerase chain reaction (RT-PCR) in fecal samples of two sporadic cases of hepatitis E in Cairo Egypt. Sequence of the complete putative structural region [open reading frame (ORF)-2] and complete region of unknown function (ORF-3) was determined for the two HEV isolates. Phylogenetic analysis of the nucleotide sequences was performed using neighbor joining or maximum parsimony methods of tree reconstruction. Direct correspondence between the HEV evolutionary trees and geographic origin of the HEV isolates was observed. Three genotypes of HEV were identified: genotype I (Asia-Africa), genotype II (US), and genotype III (Mexico). Genotype I was further divided into two subgenotypes (Asia and Africa). In the Asian subgenotype, three smaller genetic clusters were observed (China-like sequences, Burma-like sequences, and sequence from a fulminant case of HEV). The segregation of all these genetic clusters was supported by the high level of bootstrap probabilities. Four regions of the HEV genome were used for phylogenetic analysis. In all four regions, Egyptian HEV isolates were grouped in a separate African clade.

Adult↗

Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources.

The gorillas studied at Bai Hokou, Central African Republic, between August 1990 and October 1992 consumed 239 kinds of foods from 138 species of plants and invertebrates, including the fruits of 77 species. Seeds were present in 99% of all fecal samples (n = 859). Although gorillas ate fleshy fruit whenever it was available, herbaceous plants and fibrous fruits were consumed year-round and were important during times of fleshy fruit scarcity. At Bai Hokou and across their range, resources are temporally discontinuous, and western gorilla diet exhibits marked seasonal and interannual variation. Although their large body size lends them dietary flexibility relative to chimpanzees, seasonal fruit-eating shapes the foraging and ranging patterns of western lowland gorillas.

Animals↗

Reproductive events of wild cotton-top tamarins (Saguinus oedipus) in Colombia.

Reproductive patterns of wild cotton-top tamarin (Saguinus oedipus) females located in La Reserva Forestal Protectora Serranía de Coraza-Montes de María in Colosó, Colombia, were examined using long-term behavioral observations and fecal steroid analysis. Using an enzyme immunoassay, we analyzed fecal samples for E1C and PdG. Comparisons of reproductive cycles of a reproductively active female and her daughters were made. An inhibition of ovarian cycles has been observed in daughters living in their families. However, daughters also exhibited normal ovarian cycling that subsequently resulted in pregnancy. Factors influencing the fertility are discussed as they relate to the reproductive strategies of wild cotton-top tamarin females.

Animals↗

Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus).

To date, it is not known whether the seasonal occurrence of sexual behavior and mating in free-ranging Hanuman langurs at Ramnagar, Nepal, is correlated with seasonal changes in female ovarian function, and, if so, which factor(s) triggers the onset of the reproductive period. Using noninvasive fecal hormone analysis in combination with behavioral observations, this study was carried out to: 1) investigate and characterize seasonal patterns of ovarian cyclicity and timing of conception in wild langur females living in a highly seasonal habitat; and 2) examine the relationship between seasonal patterns of ovarian cyclicity, behavioral estrus, and female physical condition. Behavioral data and fecal samples were collected during a total period of 14 months from nine females living in a multi-male group. Physical condition of the females was assessed monthly by visual inspection, using a seven-fold scale. Ovulatory cycles and timing of conceptions were identified by the measurement of immunoreactive pregnanediol glucuronide (iPdG) in extracted feces. Hormone profiles in individual females revealed a clearly seasonal distribution in the occurrence of ovulatory cycles, which were restricted to the period from July to October. The distribution of female estrus behavior showed a similar seasonal pattern, and in total 88.2% of all estrus periods observed in the focal females were accompanied by ovulation. Onset of ovarian cycles as well as mating activities were strongly correlated with the onset of the rainy season. Females conceived, on average, in their second ovulatory cycle (pregnancy length: 211.6 +/- 3.4 days), with timing of conception being confined to the months when animals showed an improved physical condition. Collectively the present data clearly suggest that in seasonally-breeding langurs at Ramnagar, ecological conditions (rainfall, food availability, and quality) influence the onset of ovulations and timing of conceptions.

Animals↗

Health evaluation of translocated free-ranging primates in French Guiana.

Among over 40 mammal species threatened by the filling of a hydroelectric dam reservoir in French Guiana, three species of primates have been translocated, comprising 124 red howler monkeys, six white-faced sakis, and 95 golden-handed tamarins. Health status of the animals was evaluated by direct physical examination and by hematological, biochemical, virological, and parasitological surveys of collected blood. The physical condition of the howlers was slightly worse toward the end of the capture period, but that of sakis and tamarins remained satisfactory. Several ectoparasites (ticks, larvae of dipterous insects, fleas, and lice) were collected, and various wounds, apparently nondebilitating, were recorded in howlers. Hematological and biochemical profiles determined for the three species revealed a slight anemia in howlers. Entamoeba, Strongyloides, and Trypanoxyurus were common in fecal samples of howlers. A survey of blood smears from the three species revealed infection by several types of microfilaria, Trypanosoma rangeli-like and Plasmodium brasilianum in all three, and Trypanosoma cruzi-like in howlers. These infections had no significant impact on the health status or the hematological profiles. Serologic investigations revealed occasional reactions against Toxoplasma gondii, a strong anti-Plasmodium response in the two Cebidae species, and a weaker one in tamarins. Attempts to isolate arbovirus failed, but antibody responses to Mayaro and yellow fever viruses were strong, especially in the howlers. A strong correlation between age and serological status led to a better understanding of the epidemic cycles. Our survey indicates French Guianan primates are reservoirs for several anthropozoonoses, including malaria, Chagas disease, and arboviruses.

Animal Diseases↗

Single-copy nuclear DNA sequences obtained from noninvasively collected primate feces.

Noninvasively collected primate feces have been shown to provide a useful source of mitochondrial DNA for sequencing and nuclear microsatellite DNA for size analysis. In this study, single-copy nuclear DNA sequences were obtained from noninvasively collected fecal samples of two species of wild tamarins, Saguinus fuscicollis and S. mystax, in the context of a project on the functional utility of color vision. Noninvasive genotyping of the X-linked opsin gene is important for future studies of selection and adaptation at this locus in a number of primate species. The wide range of techniques that can now be applied successfully to DNA extracted from feces introduces a broad spectrum of potential genetic studies that can be undertaken on primates, without the need for intrusive or invasive methods.

Animals↗

Prevalence of enteric parasites in pet macaques in Sulawesi, Indonesia.

On the Indonesian island of Sulawesi, nonhuman primate pets come into frequent contact with humans, presenting the possibility of zoonotic and anthropozoonotic disease transmission. We collected fecal samples from 88 pet macaques representing six of the seven macaque species currently recognized as endemic to Sulawesi (Macaca nigra, M. nigrescens, M. hecki, M. tonkeana, M. maura, and M. ochreata) as well as two non-endemic species (M. fascicularis and M. nemestrina) in order to determine the prevalence of intestinal parasitic infection in this population. Seven taxa of intestinal protozoa (Blastocystis hominis, Iodamoeba bütschlii, Entamoeba coli, Entamoeba hartmanni, Chilomastrix mesnili, Endolimax nana, and Retortamonas intestinalis) and three taxa of nematodes (hookworm, Trichuris spp., and Ascaris spp.) were detected. The overall parasitization rate was 59.1%. Commensal organisms predominated in this population. Parasitization was not statistically correlated with macaque age group, sex, species, or location, or with the owner's level of education. These findings are discussed in the context of primate pet ownership practices in Sulawesi.

Animals↗

Effects of group dynamics and diet on the ranging patterns of a western gorilla group (Gorilla gorilla gorilla) at Bai Hokou, Central African Republic.

This study describes how group dynamics and diet have influenced the ranging patterns of a western gorilla group at Bai Hokou, Central African Republic. The results are compared with those from an earlier study [Cipolletta, International Journal of Primatology, 2003], when the same group was larger and undergoing the process of habituation to humans. Data were obtained from maps of the gorillas' travel routes, direct observations, and analysis of fecal samples. Through the years, the group has experienced a decrease in size, from eight to three individuals, with periods of membership fluctuation. The male's search for new mates resulted in a larger home range than was recorded when the group consisted of more individuals. Moreover, despite an average group size of three throughout this study, the monthly range and mean daily path length (DPL) were also larger when the group was acquiring/losing members in new areas, than when no new members joined or left the group. Fruit was consumed year-round, although more heavily so during wet months. The influence of fruit consumption on the ranging patterns was concealed initially by the effect of habituation [Cipolletta, International Journal of Primatology, 2003], and later (at least partially) by the male's search for new mates. In the last 14 months of the study, when the group numbered only three individuals and was ranging in a restricted area, the average DPL, but not the monthly range, increased when the gorillas were consuming more fruit.

Animals↗

Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia).

The steroid hormone cortisol has been associated with different levels of "stress" as well as different reproductive conditions in many primates. In callitrichids, cortisol has more often been reflective of female reproductive status than of chronic stress. In this study, we addressed the hypothesis that wild golden lion tamarin (Leontopithecus rosalia) females, whose social structure is characterized by low aggression and high social support, would not show rank ("stress")-related differences in glucocorticoids but would show reproductive changes. We collected 710 fecal samples from 22 adult females in Poço das Antas Reserve, Brazil, and nearby reintroduction areas, and assayed them for cortisol. Differences in cortisol levels were found between different reproductive conditions. Females in the first trimester of pregnancy had lower cortisol levels than nonpregnant females, although we did not differentiate between basal and ovulating levels in nonpregnant females. Cortisol rose in the third trimester of pregnancy. Primiparous females had a higher rise in the third trimester than multiparous females. No differences in cortisol levels were found among dominant females, ovulatory subordinate females, or anovulatory subordinate females. These results are similar to those obtained in other studies of callitrichid females. The lack of differences in cortisol excretion between dominants and subordinates is likely due to the low levels of overt aggression and the high level of social support available to subordinate females.

Animals↗

Behavioral strategies and hormonal profiles of dominant and subordinate common marmoset (Callithrix jacchus) females in wild monogamous groups.

New insights into the mating systems of common marmosets suggest that they are mainly monogamous, although polygyny and polyandry occasionally occur. Long-term monitoring of wild common marmosets has shown that some reports of polygynous groups (i.e., groups that contain more than one reproducing female) in fact indicate an unbalanced reproductive output associated with extragroup copulation. In this study we describe the behavioral and hormonal profiles of common marmoset (Callithrix jacchus) females living in three wild monogamous groups (Q, PBf, and T), varying from five to 11 individuals, at Nísia Floresta field station, RN, Brazil. The mating system of the groups was previously characterized in terms of affiliative, sexual, and mate-guarding behaviors. Behavioral data were collected once a week, and fecal samples were collected at least twice a week for 10-16 months, depending on the group. A preferential allogrooming relationship was recorded between dominant males and females. Under field conditions the reproductive inhibition of subordinate females appears to be more behavioral than hormonal, since subordinate females of the three groups ovulated and two conceived during the study. In these cases, the subordinate and dominant females reproduced 1 month apart, and infanticide (one case confirmed and one suspected) appeared to be part of the reproductive strategy of dominant females. Following the infanticide, ovarian inhibition (group T) or emigration and return to the natal group (group PBf) were observed. In the third group (Q) the subordinate female showed hormonal profiles compatible with pregnancy, but no infants were seen. These findings reflect the different alternatives that wild subordinate common marmoset females use to reproduce.

Animals↗

Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons.

Studies on the relationship between female testosterone (T) measures and behavior, particularly in free-ranging primate populations, remain scant. In this study we used fecal steroid analysis to examine the effects of seasonal, reproductive, and social factors on female T in a group of free-ranging hybrid baboons (Papio sp.) in the Awash National Park of Ethiopia. We collected behavioral and hormonal data from 25 adult females across an 11-month period. Solid phase extraction and radioimmunoassay (RIA) techniques were used to quantify T in 776 fecal samples collected weekly from each female. The results indicate that 1) the females had elevated T during pregnancy and during the wet season relative to other periods, 2) female dominance rank was positively related to T measures, and 3) female T and aggression were positively related within subjects but not across subjects. Higher T concentrations during pregnancy are consistent with other published profiles of pregnancy in primates. In combination with data on foraging, wet season increases in T may indicate contest competition for females. The rank-T relationship may be mediated by supplants or aggression. Finally, we discuss the different interpretations of the hormone-behavior relationship based on within- and across-subject analyses.

Aggression↗

Use of a tool-set by Pan troglodytes troglodytes to obtain termites (Macrotermes) in the periphery of the Dja Biosphere Reserve, southeast Cameroon.

At the northern periphery of the Dja Biosphere Reserve (southeastern Cameroon) we recorded a new use of a tool-set by Pan troglodytes troglodytes to prey on Macrotermes muelleri, M. renouxi, M. lilljeborgi, and M. nobilis. We recovered 79 puncturing sticks and 47 fishing probes at 17 termite nests between 2002 and 2005. The mean length of the puncturing sticks (n = 77) and fishing probes (n = 45) was 52 cm and 56 cm, respectively, and the mean diameter was 9 mm and 4.5 mm, respectively. Sixty-eight percent of 138 chimpanzee fecal samples contained major soldiers of four Macrotermes species. The chimpanzees in southeastern Cameroon appeared to be selective in their choice of plant material to make their tools. The tools found at our study site resemble those from other sites in this region. However, in southeastern Cameroon only one tool-set type was found, whereas two tool-set types have been reported in Congo. Our study suggests that, along with the different vegetation types and the availability of plant material around termite nests, the nest and gallery structure and foraging behavior of the different Macrotermes spp. at all Central African sites must be investigated before we can attribute differences in tool-use behavior to culture.

Animals↗

Molecular analyses of the intestinal microbiota of chimpanzees in the wild and in captivity.

Little information is available regarding the intestinal bacteria of chimpanzees in the wild, due to the technical difficulties of studying intestinal bacteria in the field. In this study, molecular-based bacterial analyses were performed to overcome this difficulty because polymerase chain reaction (PCR)-based methods, such as temperature gradient gel electrophoresis (TGGE) and amplified ribosomal DNA restriction analysis (ARDRA), of the bacterial 16S rRNA gene can be applied to ethanol-fixed fecal samples. The common presence of bacteria belonging to the Clostridium rRNA sub-group XIVa, such as Ruminococcus obeum and Eubacterium sp., was indicated for Bossou wild chimpanzees by ARDRA. TGGE on partial 16S rDNA followed by hierarchical clustering analysis showed a systematic difference in the composition of intestinal microbiota between wild and captive chimpanzees. However, several TGGE bands commonly shared by wild and captured chimpanzees were excised, and their sequences were obtained. They were suggested to be the Clostridium leptum subgroup bacteria, Lactobacillus gasseri-like bacterium, and Bifidobacterium pseudocatenulatum- or B. catenulatum-like bacterium. These may be considered as common intestinal bacteria for chimpanzees, and may be transmitted vertically over generations.

Animals↗

Behavior and endocrine concentrations do not distinguish sex in monomorphic juvenile howlers (Alouatta palliata).

Behavioral observations on juvenile mantled howlers are limited by visually undifferentiated genitalia; however, animals can be sexed when they are very young or if they are captured. Behavioral data and fecal samples from juveniles during month-long field studies from 1993 to 1995 were analyzed to determine whether there are developmental differences in behavior or hormone concentrations that can be used to differentiate males from females. The subjects were juveniles of known sex and age from five different social groups on Hacienda La Pacifica, Costa Rica. Based on 749.8 hr of focal-animal sampling, there were no sex differences in daily activity patterns. There were no sex differences in proximity to mothers and other group members, and age differences reflected howler life-history patterns. There were no differences in estradiol or testosterone concentration by age or sex. Juvenile monomorphy thus extends beyond morphology to behavioral and hormonal similarity as well. Most juveniles are forced out of their natal groups and remain solitary until they join new groups by supplanting all same-sex adult group members. Monomorphy may allow them to spend more time in natal groups, and thus both reduce the solitary period and allow the juveniles to improve social skills needed for later immigration. While this strategy may benefit juvenile howlers, it remains a problem for those who wish to study juvenile sex differences from a distance.

Age Factors↗

Plant DNA sequences from feces: potential means for assessing diets of wild primates.

Analyses of plant DNA in feces provides a promising, yet largely unexplored, means of documenting the diets of elusive primates. Here we demonstrate the promise and pitfalls of this approach using DNA extracted from fecal samples of wild western gorillas (Gorilla gorilla) and black and white colobus monkeys (Colobus guereza). From these DNA extracts we amplified, cloned, and sequenced small segments of chloroplast DNA (part of the rbcL gene) and plant nuclear DNA (ITS-2). The obtained sequences were compared to sequences generated from known plant samples and to those in GenBank to identify plant taxa in the feces. With further optimization, this method could provide a basic evaluation of minimum primate dietary diversity even when knowledge of local flora is limited. This approach may find application in studies characterizing the diets of poorly-known, unhabituated primate species or assaying consumer-resource relationships in an ecosystem.

Animals↗