Radiation and speciation of spider monkeys,genus Ateles,from the cytogenetic viewpoint

The chromosomes of 22 animals of four subspecies of the genus Ateles (A. paniscus paniscus, A. p. chamek, A. belzebuth hybridus, and A. b. marginatus) were compared using G/C banding and NOR (nucleolar organizer region) staining methods. The cytogenetic data of Ateles in the literature were also used to clarify the phylogenetic relationships of the species and subspecies and to infer the routes of radiation and speciation of these taxa. Chromosomes 6 and 7 that showed more informative geographic variation and the apomorphic form 4/12, exclusively in A. p. paniscus, are the keys for understanding the evolution, radiation, and specification of the Ateles taxa. The ancestral populations of the genus originated in the southwestern Amazon Basin (the occurrence area of A. paniscus chamek) and spread in the Amazon Basin and westward, crossing the Andes and colonizing Central America and northwesternmost regions of South America. The evolutionary history of the northern South American taxa is interpreted using the model of biogeographical evolution postulated by Haffer [Science 185:131–137, 1969]. Ateles paniscus paniscus is the genetically most differentiated form and probably derives from A. belzebuth hybridus. Based on the karyotype differences, the populations of Ateles can be divided into four different group. These findings indicate the necessity of a more coherent taxonomic arrangement for the taxa of Ateles. Am. J. Primatol. 42:167–178, 1997. © 1997 Wiley-Liss, Inc.     

Intrasexual selection and group spawning in quacking frogs (Crinia georgiana)

In the Australian frog Crinia georgiana, matings frequentlyinvolve a single female and multiple males (group spawning).The aim of the present study was to demonstrate a connectionbetween variation in the intensity of intrasexual competition,measured by using male density and operational sex ratio (OSR),and the incidence of group spawning. Over a 3-month breedingperiod, male density and OSR varied substantially and were significantlyinfluenced by climatic conditions. The frequency of agonisticinteractions between males was higher in denser choruses. Fightswere typically over the possession of sites used to broadcastadvertisement calls and were almost always won by larger males.At higher densities, males allocated significantly less timeto calling to attract females and spent more time as nonmovingsatellites or roaming through an aggregation (searching). However,large males always called more than did small males. The numberof males involved in a spawning correlated positively with variationin both male density and OSR. Observation of group spawningsrevealed that they generally arose when a satellite male joineda mating pair after a female chose to mate with a calling maleor when a female was seized by a searching male and the pairwas joined by other searching males. These findings, coupledwith past research documenting costs but no benefits of multiplepaternity to females, suggest that competitively inferior malesforce group spawns.     

Immobilization and health assessment of free-ranging black spider monkeys (Ateles paniscus chamek)

Eight free-ranging black spider monkeys (Ateles paniscus chamek) were immobilized with Telazol^® in Bolivia for the purpose of radio-collaring. During this procedure, the animals received complete medical examinations, and samples were collected for health analyses. Biochemical test results varied with the degree of condition of the animals, and a variety of physical abnormalities were found. Evidence of previous infections with Leptospira sp., encephalitis virus, and yellow fever virus was found. All findings contribute to establishing baseline health values for the species. The handling of primates for research projects provides a valuable opportunity to collect health-related data and samples that can contribute to wildlife management and conservation efforts. The capture and handling of free-ranging primates is always accompanied by risk of injury or mortality. It is ethically important to maximize the amount of information gathered during these procedures. Furthermore, sharing the undesirable impacts with the scientific community enables informed decisions to be made during future project development. Am. J. Primatol. 44:107–123, 1998. © 1998 Wiley-Liss, Inc.     

Female-directed Male Aggression in Wild <Emphasis Type="Italic">Ateles geoffroyi yucatanensis</Emphasis>

Male spider monkeys direct the majority of their aggression toward adult females, and the aggressive interactions may be a form of sexual coercion. We investigated female-directed male aggression in 2 wild communities of spider monkeys (Ateles geoffroyi yucatanensis) from the Otoch Ma’ax Yetel Kooh Reserve in Yucatan, Mexico to evaluate the sexual coercion hypothesis. The aggression occurred in 2 distinct forms: physical aggression and prolonged noncontact chases. The latter appeared highly ritualized in nature and accounted for >80% of all female-directed male aggression. Rates of prolonged chases, but not physical aggression, peaked when the female target was likely cycling and were associated with male place-sniffing of the substrate previously occupied by the female target. Prolonged chases were also associated with proceptive behavior directed from the female target toward her male attacker after the chase had ceased. Our data therefore suggest that prolonged chases are sexually motivated. Prolonged chases did not result in immediate copulation, but sometimes the female victim left the subgroup to travel alone with her male aggressor, and thus prolonged chases may be a form of male intimidation to coerce females into a mating consortship. However, as prolonged chases appeared highly ritualized, the chases may also be a form of male sexual display. Further investigation of the costs incurred by female recipients of prolonged chases is therefore required before one can interpret the behavior as sexual coercion.     

Female reproductive strategies in orangutans,evidence for female choice and counterstrategies to infanticide in a species with frequent sexual coercion

Intersexual conflicts over mating can engender antagonistic coevolution of strategies, such as coercion by males and selective resistance by females. Orangutans are exceptional among mammals for their high levels of forced copulation. This has typically been viewed as an alternative mating tactic used by the competitively disadvantaged unflanged male morph, with little understanding of how female strategies may have shaped and responded to this behaviour. Here, we show that male morph is not by itself a good predictor of mating dynamics in wild Bornean orangutans but that female conception risk mediated the occurrence and quality of male–female interactions. Near ovulation, females mated cooperatively only with prime flanged males who they encountered at higher rates. When conception risk was low, willingness to associate and mate with non-prime males increased. Our results support the hypothesis that, together with concealed ovulation, facultative association is a mechanism of female choice in a species in which females can rarely avoid coercive mating attempts. Female resistance, which reduced copulation time, may provide an additional mechanism for mate selection. However, coercive factors were also important as prime males were frequently aggressive to females and females used mating strategies consistent with infanticide avoidance.     

Tropical rain forest conversion and perspectives in the conservation of wild primates (Alouatta and Ateles) in Mexico

The original distribution of the tropical rain forest and of the populations of Alouatta palliata, Al. pigra, and the two subspecies of Ateles geoffroyi in southern Mexico have been reduced by at least 90% in the last 40 years as a result of conversion of natural habitat to pasture and agricultural fields. This dramatic conversion has been caused mainly by the rapid growth of the human population in the southern states of the country. In the region of Los Tuxtlas in southern Veracruz, where the only longitudinal popululational and ecological studies of A. palliata and At. g. vellerosus have taken place, only 15% of the original extension of the tropical rain forest remains today. The intensive destruction of suitable primate habitat in this region has resulted in an accelerated process of extinction of the primate species. It is estimated that only about 200 At. g. vellerosus and about 1200 Al. palliata exist in the remaining small portion of their original habitat. Today, the distribution of the three primate species in Mexico is intensively and extensively fragmented, and only five potential foci for conservation exist in the country. Urgent action is required to protect the primate populations in the region of Los Tuxtlas and at the other four foci, as some of these populations may disappear by 1995.     

Food Preferences and Nutrient Composition in Captive Spider Monkeys,Ateles geoffroyi

We assessed the occurrence of food preferences in captive spider monkeys and analyzed whether their preferences correlate with nutrient composition. Using a two-alternative choice test, we repeatedly presented 7 Ateles geoffroyi with all possible binary combinations of 12 types of food that are part of their diet in captivity. They exhibited the following rank order of preference: avocado > sapodilla > pineapple > mango > papaya > melon > banana > apple > tomato > orange > carrot > cucumber. Correlational analyses revealed that this preference ranking is significantly positively correlated with total energy content, irrespective of the source of energy as neither total carbohydrate content nor protein or lipid content is significantly correlated with food preference. Further, food preferences are significantly negatively correlated with water content and positively correlated with the content of magnesium, copper and manganese. These results suggest that despite their high degree of frugivory and high taste sensitivity for soluble carbohydrates, spider monkeys are opportunistic feeders with regard to maximizing net gain of energy.     

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.     

Female-Directed Aggression in Free-Ranging Ateles geoffroyi

In a study of the reproductive biology and behavior of black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama, 107 instances of female directed male aggression (male attacks) occurred during >1,000 h of observation. Two hypotheses might explain this behavior. First, males may attack to induce defecation/urination by target females, from which they can gain reproductive information. Rates of defecation and urination did not increase subsequent to attacks; however, there was an association between attacks and investigative behaviors such as place sniffing. Alternatively, the attacks might be a form of sexual coercion. My results indicate that female reproductive state, as determined by fecal steroid metabolites (E1C and PdG), had an inconsistent effect on the frequency of attacks received. In addition, when females were in the peri-ovulatory period of the ovarian cycle they did not receive more attacks than at other times. Nor were attacks associated with observed copulations, suggesting that sexual coercion does not sufficiently explain the behavior. Some support is provided for the notion that the attacks allow males to dominate equally-sized females.     

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.     

Infanticide in black capuchin monkeys (Cebus apella nigritus) in Iguazú National Park, Argentina

We report here one observed and two potential cases of infanticide during a brief period of 1 month after a dominant male replacement in one group of black capuchin monkeys in Iguazú National Park, Argentina. We also compile infant disappearances and demographic data in seven groups followed from 1-14 years. Behavioral and molecular data showed that the probability that an infanticidal male would kill his own progeny is very low in this species. Females that lost infants less than 6 months old had shorter interbirth intervals than females whose infants survived (14.12 ± 5.32 months, n=17 vs. 20.42 ± 5.65 months, n=34). Females whose infants die shortly after takeovers mate with the presumed infanticidal male during the most fertile days of their subsequent estrous periods giving this male a high probability of siring the new progeny. We recorded 181 proceptive periods and 52 births from 18 adult females in two groups. Most proceptive periods were concentrated during a conception season, but there was an increase in sexual behavior after male takeovers. Seven females copulated while pregnant after the observed male takeover, an unusual behavior in this species in years of group stability. Of 24 infants born during takeover years, 62.5% did not survive the first year, whereas only 22.5% of 80 infants died in years without male replacements. We found a significant positive association between infant mortality and male takeovers, but not with food provisioning. The main cause of infant mortality in this population is associated with male takeovers. Our results suggest that infanticide can have an important effect on the behavior of this species, selecting for female behaviors that function to reduce infanticide risk.