Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi)

I report ad libitum data on 18 copulations involving free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. All copulations were performed in a dorsoventral position, as is typically reported for this genus. Intromission often appeared difficult to achieve, possibly as a result of the large size of the glans penis in these animals. The average length from intromission to termination of thrusting exceeded 17 min, followed by an average period of almost 2 min before separation occurred, which suggests the possibility of a copulatory lock. Offspring of the female participant were almost always in close proximity to or in contact with the pair, and harassment by the offspring was observed only during the final stages of the copulation. All but one copulatory event occurred in complete seclusion from other adult males, and sexual behavior was not limited to any one adult male in the group.     

Lethal intragroup aggression by adult male spider monkeys (Ateles geoffroyi)

I report three cases of coalitionary aggression by adult male black-handed spider monkeys (Ateles geoffroyi) against subadult males within their community on Barro Colorado Island (BCI), Panama. Two of these cases were followed by the disappearance and presumed death of the victim. Similar behavior was recently reported by Valero et al. [in press], who suggested that this behavior may be the result of intense male reproductive competition. Like the single instance they reported, the cases I report all occurred when the operational sex ratio was approximately 1:1, which suggests that intense competition among males for access to reproductively viable females may be a contributing factor. Additionally the very low density of spider monkeys on BCI may play a significant role in the occurrence of this lethal aggression. Large numbers of adult males are not necessary to protect a territorial boundary against neighboring groups, and additional males may act merely as mating competition.     

Gustatory Responsiveness to food-associated acids in the spider monkey (Ateles geoffroyi)

The gustatory responsiveness of four adult spider monkeys to five food-associated acids was assessed in two-bottle preference tests of brief duration (3 min). The animals were given the choice between a 30 mM sucrose solution and defined concentrations of citric acid, ascorbic acid, malic acid, acetic acid, or tannic acid dissolved in a 30 mM sucrose solution. With this procedure,Ateles geoffroyi was found to significantly discriminate concentrations as low as 5 mM ascorbic acid, citric acid, and acetic acid, 10 mM malic acid, and 0.1 mM tannic acid from the alternative stimulus. With the latter two substances, the monkeys rejected all suprathreshold concentrations tested, whereas with the former three substances, the animals showed an inverted U-shaped function of preference, i.e. they rejected high concentrations, but significantly preferred low but detectable concentrations of these acidic tastants over the alternative sweet stimulus. The results showed (1) the spider monkey to respond to the same range of acid concentrations as other nonhuman primate species; (2) thatAteles geoffroyi, is able to detect food-associated acids at concentrations well below those present in most fruits; and (3) that unlike most other primate species tested so far, spider monkeys do not generally reject acidic tastants but show a substanceand concentration-dependent change in responsiveness that may range from rejection to preference. The results support the assumptions that spider monkeys may use sourness and/or astringency of food-associated acids as a criterion for food selection, and that the gustatory responsiveness ofAteles geoffroyi to acidic tastants might reflect an evolutionary adaptation to frugivory.     

Effect of increasing trypsin concentrations on seminal coagulum dissolution and sperm parameters in spider monkeys (Ateles geoffroyi)

Seminal coagulum formation in spider monkeys (Ateles geoffroyi) interferes with the efficient recovery and evaluation of spermatozoa. The main objective was to assess the effect of increasing concentrations of trypsin on dissolution of seminal coagulum and spermatic parameters. Seminal coagulum was incubated at 37 °C without trypsin or in the presence of increasing trypsin concentrations (0.1%, 1.0%, and 5.0%). For each sample, coagulum dissolution time was measured, and sperm concentration, viability, motility, and morphology were evaluated using light microscopy and/or transmission electronic microscopy (TEM). Trypsin concentrations of 1.0% and 5.0% more rapidly liquefied seminal coagulum, averaging 32 and 21 min, respectively, compared with nontrypsinized controls, with maintenance of greater sperm viability (70.8% and 72.5%, respectively). Coagulum treated with 1.0% trypsin and the liquid ejaculate fraction averaged higher sperm motility (40.1% and 55.6%, respectively) than control samples, and both 1.0% and 5.0% trypsin treatment allowed recovery of increased numbers of motile spermatozoa. There was greater sperm fragmentation at the head and midpiece level after treatment with 1.0% and 5.0% trypsin (55.8% and 55.9%); however, the percentage of normal morphology in structurally intact spermatozoa did not differ relative to controls. With transmission electronic microscopy imaging, there were similar percentages of spermatozoa with plasma membrane swelling in the midpiece and acrosomal regions in trypsin-treated samples and controls. In conclusion, trypsin treatment of spider monkey seminal coagulum exerted a concentration-dependent effect on dissolution time and various spermatic parameters. Higher trypsin concentrations caused more rapid liquefaction of coagulum and recovery of greater numbers of motile spermatozoa, but may adversely affect fragmentation of spermatozoa and could compromise sperm function and cryopreservation potential.     

Relative taste preferences for food-associated sugars in the spider monkey (Ateles geoffroyi)

The purpose of the present study was to determine relative taste preferences for five food-associated sugars inAteles geoffroyi. Using two-solution choice tests of brief duration (5 min) four adult spider monkeys were given the choice between all binary combinations of sucrose, fructose, glucose, lactose, and maltose presented in equimolar concentrations of 20, 50, 100, and 200 mM respectively. Preferences for individual sugars were stable across the concentrations tested and indicate an order of relative effectiveness (sucrose>fructose>glucose≥lactose≥maltose) which is similar to results obtained with the same method in the squirrel monkey and to findings on relative sweetness in man. These results support the assumption that the order of relative effectiveness of the sugars under investigation found in the present study may represent a general pattern of preference in frugivorous and perhaps all primates.     

Alloparental behavior in a captive group of spider monkeys (Ateles geoffroyi) at the Auckland zoo

I studied alloparental behavior in a captive group of spider monkeys at the Auckland Zoo using seven infants as focal subjects and assessed the effects of age, sex, and reproductive status of alloparents on patterns of infant-other interaction. Adult males initiated interactions with infants most often, followed by adult females. Immature individuals interacted with infants infrequently. Infants themselves initiated contact with adult males more often than with other members of the group. Alloparental behavior in spider monkeys differs from that in most other species in that the infant is an active rather than a passive participant in alloparental interactions. I discuss the patterns of infant-other interaction in relation to the social structure and dispersal patterns of Ateles.     

Gustatory thresholds for food-associated sugars in the spider monkey (Ateles geoffroyi)

The purpose of this study was to determine gustatory thresholds for five different food-associated sugars in Ateles geoffroyi. Using a two-bottle test, three adult spider monkeys were found to significantly prefer concentrations as low as 3 mM sucrose, 15 mM fructose, 20 mM glucose, and 10 mM lactose over tap water. Maltose was significantly discriminated down to 20 mM with individual animals showing either a preference or an aversion, or an inverted U-shaped function of preference toward higher concentrations of this carbohydrate. The results showed the spider monkey to respond to lower sugar concentrations compared to other nonhuman primates tested so far and thus support the assumptions that Ateles geoffroyi may use sweetness as a criterion for food selection, and that the remarkably high sweet-taste sensitivity of this frugivorous species might be correlated with its dietary specialization. © 1996 Wiley-Liss, Inc.     

Fecal analysis of ovarian cycles in female black-handed spider monkeys (Ateles geoffroyi)

An enzyme immunoassay (EIA) was applied to characterize the reproductive endocrinology of adult female black-handed spider monkeys (Ateles geoffroyi). Analysis of paired urine and fecal samples, collected from two females housed at San Diego Zoo, confirmed that the EIAs employed provided quantitative measurements of ovarian sex steroid hormones. Fecal metabolite levels were significantly correlated with those in urine, confirming that feces are a valid source of steroid metabolites in this species. The excretion of these metabolites in feces lagged urinary excretion by 1-2 days. The ovarian cycle profiles of the two captive females and five free-ranging females are comparable, with an average length of approximately 20-23 days. Cyclical bleeding, as previously reported, was observed in one of the two captive females. Pregnancy was detected in four free-ranging females, and early fetal loss for one female was indicated by hormonal data.     

Social responses to the traumatic injury of a juvenile spider monkey (Ateles geoffroyi)

The behavioural development of a juvenile male spider monkey (Ateles geoffroyi) preceding and subsequent to a traumatic injury resulting in the loss of his tail, was documented over a nine-month period in Santa Rosa National Park, Costa Rica. The juvenile became heavily reliant on his mother, who readily provided compensatory care, including nursing the juvenile even though he had previously been weaned. In comparison to another juvenile male spider monkey of similar age, the development of the injured animal was severely retarded and even five months after the accident, the juvenile was still nursing and being carried by his mother. As injuries may be relatively common among primates it is suggested that the provision of compensatory care is an important trait in many primate species.     

Grooming,kinship, and co‐feeding in captive spider monkeys (Ateles geoffroyi)

Allo‐grooming is perhaps the most powerful affiliative behavior observed in non‐human primates. However, the functional significance of grooming in New World monkeys has not yet been fully understood, perhaps because grooming is less frequently observed in platyrrhines. To differentiate the potential role of affiliative investment and/or kinship on sharing access to food (co‐feeding) in spider monkeys, behavioral data on grooming, embracing, and feeding were collected from two different groups of captive study subjects: a familiar/kin group and a non‐familiar/non‐kin group. The results of this study suggest that family‐related spider monkeys that engage in grooming tend to share access to food resources more than unfamiliar conspecifics that do not groom. One explanation for this difference is that the unfamiliar study subjects had not yet invested in the affiliative social network, were not reciprocating their affiliative investments and hence, had a higher tendency toward single animal monopolizing resources. Degree of relatedness alone was not found to be a determinant for sharing the access to food, suggesting that familiarity in spider monkeys is based on the extent to which animals invest in affiliative relationships. In this study, only animals that had engaged in long‐term grooming and recognized each other as familiar shared the access to food. Therefore, it might be likely that in spider monkeys, long‐term grooming of high intensity has to be developed for co‐feeding to occur. Zoo Biol 20:293–303, 2001. © 2001 Wiley‐Liss, Inc.     

Diet of spider monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge and future directions

Here we review all published articles and book chapters, as well as unpublished theses and data of Ateles geoffroyi diet to (1) summarize the literature; (2) synthesize general feeding patterns; (3) document plant taxonomic similarity in diet across study sites; and (4) suggest directions for future research and conservation priorities. We found 22 samples from five countries: Mexico, Guatemala, El Salvador, Costa Rica and Panama. Tropical wet forest is the most studied habitat (N=13 samples), followed by tropical dry forest (6) and tropical moist forest (3). Most samples have been carried out in large protected forests. In spite of showing an overall high dietetic diversity (364 species, 76 families), A. geoffroyi concentrated the majority of feeding time on a few species in the families Moraceae and Fabaceae. At all study sites fruits were the most common food item in the diet followed by leaves. Furthermore, a greater variety of food items and less fruit were consumed in forest fragments. These findings suggest that fruit shortage in fragments results in primates using foods of presumably lower energetic content such as leaves. Similarity in diet was higher among groups geographically closer to each other than among distant groups, showing that the floristic and phenological characteristics of the forest can influence diet composition. We conclude that several years of data are required to fully describe the dietary list of A. geoffroyi at any one site, as studies of the same group over different years shared as little as 56% of species. As most populations of A. geoffroyi live in highly fragmented landscapes, it is crucial to carry out studies in these areas to evaluate (1) changes in diet and activity patterns that may negatively affect survival; and (2) habitat attributes that may favor their persistence in altered landscapes.     

Grooming behavior of spider monkeys (Ateles geoffroyi) on barro colorado Island,Panama

Quantitative grooming data are presented for free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Republic of Panama. A total of 126 grooming sessions was recorded, with an average session length of 2.0 min (range, 0.1 to 10.0 min). Grooming was an infrequent behavior; on average, individuals allocated only 2.5% of their daily activity to grooming. Two daily peaks of grooming activity were observed, one near midday and another in the late aftermoon between 1600 and 1700. Adult females groomed most frequently, followed by males and then juveniles. Juveniles were the most frequent recipients of grooming, followed by females and then males. Individual preferences were observed primarily between mother-offspring, male-male, and juvenile-male grooming partners in this male-bonded fission-fusion, species. Grooming interactions reflect many of the social characteristics of spider monkey societies: intraclass grouping preferences, long period of juvenile dependence, male philopatry, and female dispersal.     

Sperm quality differences between the rainy and dry seasons in captive black-handed spider monkeys (Ateles geoffroyi)

The present work provides an assessment of sperm measures (concentration, motility, viability, etc.) of three black-handed spider monkeys (Ateles geoffroyi) during the rainy and dry seasons in Mexico City, as well as an evaluation of the between-subjects variability of sperm quality. Twenty samples obtained by rectal electroejaculation and digested with trypsin were evaluated. The results showed that during the dry season (n = 9) the semen samples were of better quality than those obtained during the rainy season (n = 11). The individual animals showed differences in sperm concentration, although there were no differences in sperm quality.     

Sex differences in the social behavior of wild spider monkeys (Ateles geoffroyi yucatanensis)

Competition for resources and the need for cooperation are reported to affect patterns of social interactions and thus the quality of social relationships in primates. Relationships may be described as high quality when both individuals behave in a way that benefits their partner. We investigated the distribution of a wide range of social behaviors across sex partner combinations of adult spider monkeys with specific reference to contested resources. Data were collected from two communities of wild spider monkeys (Ateles geoffroyi yucatanensis) in the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico. Affiliative behavior was exchanged most frequently between males, and as male-male aggression was rare, male-male social relationships were characterized as high quality. Female-female social relationships were best described as low quality as females showed no preference to be in proximity with other females and female-female affiliative behavior was rare. Relationships between the sexes generally were characterized by high rates of female-directed male aggression, although additional investigation into the effects of kinship and female reproductive state on male-female relationships is required before further conclusions can be drawn. Dyadic and coalitionary female-female aggression was significantly higher than expected in a feeding context, confirming that female spider monkeys primarily compete for access to food. Male-male aggression did not increase significantly when in the presence of females, but males embraced at higher rates when in mixed-sex subgroups. As embraces serve to reduce the likelihood of aggression during tense situations, high rates of male-male embraces in mixed-sex subgroups may mitigate male conflicts over access to females.     

The menstrual cycle of the spider monkey (Ateles geoffroyi)

The ovarian cycles of four adult female spider monkeys (Ateles geoffroyi) were followed daily throughout 30 days by means of vaginal swabs and blood samplings. Cytological analyses of the vaginal swabs and radioimmunoassay determination of the daily levels of estradiol-17β (E₂) and progesterone (P₄) were done in order to classify the kind of ovarian cycle of this species. Our results show that Ateles geoffroyi females display menstrual cycles of about 24 days on average. By comparison with the well-known menstrual cycles of women, apes, and Old World monkeys, the four distinctive cytological phases (bleeding, follicular, periovulatory, and luteal) could be recognized; mid-cycle E₂ peaks followed by mid-luteal increases of the same hormone were present in all four females. P₄ levels were higher after the E₂ peak, although both hormones were present throughout the cycles. Also, age-dependent features, hormone profiles, and changes in menstrual phases lengths were detected. Am. J. Primatol. 44:183–195, 1998. © 1998 Wiley-Liss, Inc.     

Developmental pattern of the bony tentorium of spider monkeys (Ateles)

Based on their developmental patterns, the bony tentorium (BT) and bony falx (BF) of mammals can be classified into two types, the carnivoran type and the dolphin type. The former develops as part of the skull bones during the fetal period and is already completed at birth, while the latter is gradually formed by ossification in the tentorium cerebelli (TC) and falx cerebri (FC) during the course of aging. The BT of spider monkeys is assigned to the dolphin type.     

Aging-related reproductive decline in the male spider monkey (Ateles geoffroyi)

Background It is unknown whether male black‐handed spider monkeys (Ateles geoffroyi) undergo a reproductive decline as they age. The purpose of this work was investigating whether serum testosterone and semen quality decrease with age in these primates as occur in other species. Methods In this study, we assessed age variations in the concentration of serum testosterone, sperm counts, and motility in nine males. We took serum blood samples and semen samples by electroejaculation of anesthetized males throughout the fertile season. Results We found that testosterone levels and total sperm concentration, motile, progressive, fast linearly moving, medium linearly moving, slow linearly moving and immotile sperm significantly decreased with age. Conclusions Our results show that a reproductive decline occurs in male spider monkeys because of a decrease in sperm counts. These results are similar to those of rhesus monkeys and men, despite the phylogenetic distance between New and Old World primates.     

Demography,ranging patterns,and activity budgets of black spider monkeys (Ateles paniscus chamek) in the Manu National Park,Peru

Results of a long-term field study on the ecology and social organization of two groups of black spider monkeys (Ateles paniscus chamek) in Peru are reported. Demography, ranging patterns, and activity budgets provide insight into some of the proximate determinants of fission-fusion social organization in this species and illustrate the different strategies used by males and females to gain access to critical resources. Longitudinal data on known individuals provide evidence for male natal philopatry and female emigration at sexual maturity in this population. Interbirth intervals are long (mean = 34.5 months) in comparison with most other primate species, and 5 of 15 infants seen within a few days of birth died or disappeared before they were a year old. Home ranges are large (150–250 ha) and fairly discrete; overlap with neighboring groups is on the order of 10–15%. Males and females differed substantially in their ranging patterns; females, particularly those with infants, restricted much of their ranging to a “core area” 20–33% the size of the total group range, whereas males ranged more evenly over the entire area occupied by the group. Daily path length varied over almost an order of magnitude from 465 m to 4,070 m, with a mean of 1977 m. Males spent more time traveling and less time feeding than most females. These results are compared with those obtained in previous studies of Ateles and with similar data from other primate species to assess their implications for the evolution of fission-fusion sociality in spider monkeys. The ecological factors responsible for the evolution of very similar social organizations in spider monkeys and chimpanzees are discussed.     

Relationship quality affects fission decisions in wild spider monkeys (Ateles geoffroyi)

Fission–fusion dynamics are thought to be mainly a response to differential availability of food resources. However, social factors may also play a role. Here, we examined whether the quality of social relationships between group members affects fission decisions. During 21 months, we collected data on social interactions and fission events of 22 spider monkeys (Ateles geoffroyi) living in a community in the protected area of Otoch Ma'ax Yetel Kooh, Yucatan, Mexico. By entering seven indexes of social interactions into a principal component analysis, we obtained three components of relationship quality, which we labelled “compatibility,” “value” and “insecurity” given the relative loadings of the indexes. Our results showed that individuals were more likely to fission into the same subgroup with community members with whom they shared higher levels of compatibility and value and lower levels of insecurity. In addition, individuals preferred to fission into the same subgroup with same‐sex group members, as expected based on what is known for the species. Our findings highlight the role of social factors in fission decisions. Adjustments in subgroup size are based on multifaceted social preferences, incorporating previously unexamined aspects of relationship quality, which are independent from overall levels of affiliative interactions.