Infanticide and cannibalism by male chimpanzees at Ngogo, Kibale National Park, Uganda

Researchers have documented infanticide by adult males in four wild chimpanzee populations. Males in three of these have killed infants from outside of their own communities, but most infanticides, including one from Kanyawara, in Kibale National Park, Uganda, took place within communities. Here we report two new cases of infanticide by male chimpanzees at a second Kibale site, Ngogo, where the recently habituated chimpanzee community is the largest yet known. Both infanticides happended during boundary patrols, which occur at a high frequency there. Patrolling males attacked solitary females who were unable to defend their infants successfully. The victims were almost certainly not members of the Ngogo community. Males cannibalized both infants and completely consumed their carcasses. These observations show that infanticide by males is widespread in the Kibale population and that between-community infanticide also happens there. We discuss our observations in the context of the sexual selection hypothesis and other proposed explanations for infanticide by male chimpanzees. The observations support the arguments that infanticide has been an important selective force in chimpanzee social evolution and that females with dependent infants can be at great risk near range boundaries, but why male chimpanzees kill infants is still uncertain.     

Towing the party line: territoriality, risky boundaries and male group size in spider monkey fission-fusion societies

Spider monkey communities are classic fission-fusion primate societies. I present data suggesting that spider monkeys (Ateles chamek) at Lago Caiman are territorial; adult males traveled further and faster than adult females and subgroup size was significantly higher in boundary areas of the spider monkey territory where intercommunity disputes were observed than in non-boundary areas. I then go on to examine data from 20 Ateles communities distributed across 14 study sites and five species to investigate how a series of demographic, ecological and geographical parameters influence the number of males in a given spider monkey community. Analyses suggest that the number of males is not significantly related to the number of females in a community, the area of the community home range, or the total perimeter length of the community boundary. However, risky boundary perimeter length, or the length of perimeter that directly borders another spider monkey community, explains 88% of observed variations in the number of males in each community. I discuss the results in relation to spider monkey ecology and territoriality, as well as the potential of this relationship for explaining chimpanzee (Pan) behavior given their extremely similar fruit specialist, male philopatry, territoriality and fission-fusion social system.     

Group size and stability: Why do gibbons and spider monkeys differ?

Gibbons and spider monkeys have similar diets, body size, and locomotor patterns. They are therefore expected to be subject to similar socioecological rules. However their grouping patterns differ. Gibbons live in small stable groups, whereas spider monkey form unstable sub-groups that vary from small to large during different seasons. If similar principles apply to the two species, food abundance should vary more for spider monkeys than for gibbons; food density should be similar for the two species when spider monkey sub-groups are the same size as gibbon groups; and the highest level of food abundance should be higher for spider monkeys than for gibbons. These predictions are upheld for a comparison of particular populations ofHylobates muelleri andAteles geoffroyi.     

Reproductive Parameters of Wild Female Lagothrix lagotricha

I describe the reproductive patterns of female woolly monkeys (Lagothrix lagotricha) based on a 12-year study of one group of them at Macarena Ecological Investigations Center, Meta, Colombia. As in other atelin species—muriquis and spider monkeys—characterized by male philopatry, female woolly monkeys leave their natal groups. The age of emigration is ca. 6 years. Females probably begin to copulate with adult males soon after emigration, while their mean age of first parturition is 9 years. They frequently changed groups until they birthed. The average interbirth interval is 36.7 mo (n = 13). All births occurred between July and December (late wet season to early dry season). Copulation occurred throughout the year. However, they copulated more frequently in the estimated conception period from December to May (early dry season to early wet season) than in the birth season. The females had a period of sexual inactivity averaging <23.4 mo after parturition, followed by a period of sexual activity >7.2 mo until conception. The copulation period and copulation cycle or interval between copulation periods averaged 2.3 and 11.3 days calculated by a conventional method, or 3.1 and 14.7 days by a slightly modified method. The reproductive parameters of woolly monkeys are quite similar to those reported for other atelins in many respects, except the immigration process and age of first copulation.     

Patterns of injury in zoo-housed spider monkeys: A problem with males?

Aggression among wild spider monkeys is most frequently reported to occur between the sexes, with adult males directing aggression towards adult females and the aggression is normally non-injurious. After two severe instances of aggression in the group of spider monkeys housed at Chester Zoo, we developed a questionnaire to investigate the frequency, direction and possible reasons for aggression in zoo-housed spider monkeys. We sent our questionnaire to 55 zoos worldwide and obtained records from 26 groups, which yielded detailed accounts of 143 aggressive incidents: 56 events for the actors and 127 events for the targets of aggression. We found that zoo-housed spider monkeys are predominantly maintained in small social groups, with a single adult male, two adult females and their offspring. Of the aggression reported, 23.1% of incidents resulted in severe or lethal injuries. Adult males were the most frequent actors of aggression and accounted for 66.7% of incidents. Six cases of male–male aggression were lethal. The most striking pattern was that adult males directed aggression towards non-adult males more than any other age/sex category. The most frequently reported context of aggression was tension between adult and non-adult males. These findings contradict previous reports from wild spider monkeys where female-directed male aggression is most frequently reported. In light of our findings, we recommend that males form the core of the group and that females be relocated among groups to reflect the wild condition of male philopatry and female dispersal. In addition, enclosure design should allow opportunities for the monkeys to segregate themselves from other group members, simulating fission, which is a conflict management strategy for avoiding aggression in wild spider monkeys.     

Olfactory sensitivity for enantiomers and their racemic mixtures--a comparative study in CD-1 mice and spider monkeys

Using a conditioning paradigm, the olfactory sensitivity of six CD-1 mice for the enantiomers of carvone and of limonene as well as for their racemic mixtures was investigated. With all six stimuli, the animals significantly discriminated concentrations 相似文献   

New cases of inter-community infanticide by male chimpanzees at Ngogo,Kibale National Park,Uganda

Infanticide by males has been recorded in four chimpanzee populations, including that in Kibale National Park, Uganda. Some infanticidal attacks occur during inter-community aggression. The sexual selection hypothesis does not easily explain these attacks because they may not directly increase male mating opportunities. However, females in the attackers’ community may benefit by expanding their foraging ranges and thereby improving their reproductive success; thus infanticide may increase male reproductive success indirectly. We report two new cases of infanticide by male chimpanzees at Ngogo, Kibale National Park. Like two previous cases, these occurred during a boundary patrol and were almost certainly between-community infanticides. The patrolling males attacked despite the proximity of males from the victims’ presumed community. This probably explains why, unlike the earlier cases, they did not completely cannibalize their victims. Such attacks seem to be relatively common at Ngogo and infanticide may be an important source of infant mortality in neighboring communities. Our observations cannot resolve questions about the sexual selection hypothesis. However, they are consistent with the range expansion hypothesis: the infanticides occurred during a period of frequent encounters between communities associated with a mast fruiting event, and Ngogo community members greatly increased their use of areas near the attack site during another mast fruiting event one year later. Our observations contribute to growing evidence that lethal intergroup aggression is a common characteristic of wild chimpanzee populations.     

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.     

Foraging,Food Choice,and Food Processing by Sympatric Ripe-Fruit Specialists: <Emphasis Type="Italic">Lagothrix lagotricha poeppigii</Emphasis> and <Emphasis Type="Italic">Ateles belzebuth belzebuth</Emphasis>

Studies of interspecific competition and niche separation have formed some of the seminal works of ecology. I conducted an 18-mo study comparing the feeding ecologies of 2 sympatric, closely-related ripe-fruit specialists, Humboldt's woolly monkeys (Lagothrix lagotricha poeppigii), and the white-bellied spider monkeys (Ateles belzebuth belzebuth) in Amazonian Ecuador. Woolly monkeys in the terra firme forest live at roughly triple the density of spider monkeys (31 versus 11.5 animals/km²). Woolly monkeys spend 17% of their time foraging, while spider monkeys spend only 1% of their time foraging. Spider monkeys alone fed on soil and termitaria, which are rich in phosphorus. Woolly monkeys are not hard-fruit specialists. Their fruit diet is significantly more diverse than that of spider monkeys. Dietary overlap between the 2 species is high, yet each specializes to some degree on a different set of fruit resources. Woolly monkeys visit more food sources per unit of time, feed lower in the canopy, visit more small food patches, and prey on more seeds. Spider monkeys feed on fewer, richer food sources and are more than twice as likely to return to a particular fruit source than woolly monkeys are. Spider monkeys maximize fruit pulp intake, carrying more intact seeds in their guts, while woolly monkeys minimize seed bulk swallowed through more careful food processing. Surprisingly, several preferred spider monkey foods with high fat content and large seeds are avoided by woolly monkeys. I outline the different ecological dimensions involved in niche separation between the 2 species and discuss the possible impetus for their evolutionary divergence.     

有机荔枝园、常规荔枝园和天然荔枝园蜘蛛类群的比较

2004～2005年,对珠海市斗门区有机、常规和天然荔枝园的蜘蛛群落进行了系统的调查和分析,结果表明,不同类型荔枝园蜘蛛群落丰富度S值天然＞有机＞常规荔枝园;多样性指数H'值有机＞天然＞常规荔枝园;均匀度E值有机＞天然＞常规荔枝园.说明进行有机管理的荔枝园对蜘蛛群落的多样性影响较小,有利于保护和发挥天敌的自然控制力.有机、常规荔枝园的优势类群均为园蛛科、皿蛛科和球蛛科,而天然荔枝园除这三者外,跳蛛科也明显增加.除天气因素外,更重要的还与人为农事活动干扰程度直接相关.有机荔枝园不使用化学农药,蜘蛛种类多,个体数也较多.而常规荔枝园由于频繁地使用了化学合成物质,蜘蛛种类和数量较少.说明施用大量的化学农药,对蜘蛛的影响较大.     

Influence of climatic variables, forest type, and condition on activity patterns of Geoffroyi's spider monkeys throughout Mesoamerica

Understanding how species cope with variations in climatic conditions, forest types and habitat amount is a fundamental challenge for ecologists and conservation biologists. We used data from 18 communities of Mesoamerican spider monkeys (Ateles geoffroyi) throughout their range to determine whether their activity patterns are affected by climatic variables (temperature and rainfall), forest types (seasonal and nonseasonal forests), and forest condition (continuous and fragmented). Data were derived from 15 published and unpublished studies carried out in four countries (Mexico, El Salvador, Costa Rica, and Panama), cumulatively representing more than 18 years (221 months, >3,645 hr) of behavioral observations. Overall, A. geoffroyi spent most of their time feeding (38.4 ± 14.0%, mean ± SD) and resting (36.6 ± 12.8%) and less time traveling (19.8 ± 11.3%). Resting and feeding were mainly affected by rainfall: resting time increased with decreasing rainfall, whereas feeding time increased with rainfall. Traveling time was negatively related to both rainfall and maximum temperature. In addition, both resting and traveling time were higher in seasonal forests (tropical dry forest and tropical moist forest) than in nonseasonal forests (tropical wet forest), but feeding time followed the opposite pattern. Furthermore, spider monkeys spent more time feeding and less time resting (i.e., higher feeding effort) in forest fragments than in continuous forest. These findings suggest that global climate changes and habitat deforestation and fragmentation in Mesoamerica will threaten the survival of spider monkeys and reduce the distributional range of the species in the coming decades. Am. J. Primatol. 73:1189–1198, 2011. © 2011 Wiley Periodicals, Inc.     

Polygynandry,face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae)

The Hihi or Stitchbird Notiomystis cincta breeding system is highly variable and includes monogamy, polyandry, polygyny and polygynandry. Males have large testes (4.2% of body mass), very large numbers (1460 × 10⁶) of sperm in their seminal glomera and an unusually enlarged cloacal protuberance. These features are also found in other species with highly variable mating systems where males are under intense sperm competition. Hihi copulate in two different positions: face to face and, more conventionally, with the male on the female's back. Face-to-face copulation is unique among birds and appears to be a form of forced copulation. The presence of enlarged cloacas in both sexes could aid the transfer of sperm. Both male and female Hihi appear to benefit from a mixed reproductive strategy where a female Hihi can solicit copulations from males other than her partner and male Hihi can perform extra-pair copulations both with willing females or by forced copulation.     

Sleeping Sites and Latrines of Spider Monkeys in Continuous and Fragmented Rainforests: Implications for Seed Dispersal and Forest Regeneration

Spider monkeys (Ateles geoffroyi) use sites composed of one or more trees for sleeping (sleeping sites and sleeping trees, respectively). Beneath these sites/trees they deposit copious amounts of dung in latrines. This behavior results in a clumped deposition pattern of seeds and nutrients that directly impacts the regeneration of tropical forests. Therefore, information on the density and spatial distribution of sleeping sites and latrines, and the characteristics (i.e., composition and structure) of sleeping trees are needed to improve our understanding of the ecological significance of spider monkeys in influencing forest composition. Moreover, since primate populations are increasingly forced to inhabit fragmented landscapes, it is important to assess if these characteristics differ between continuous and fragmented forests. We assessed this novel information from eight independent spider monkey communities in the Lacandona rainforest, Mexico: four continuous forest sites and four forest fragments. Both the density of sleeping sites and latrines did not differ between forest conditions. Latrines were uniformly distributed across sleeping sites, but the spatial distribution of sleeping sites within the areas was highly variable, being particularly clumped in forest fragments. In fact, the average inter-latrine distances were almost double in continuous forest than in fragments. Latrines were located beneath only a few tree species, and these trees were larger in diameter in continuous than fragmented forests. Because latrines may represent hotspots of seedling recruitment, our results have important ecological and conservation implications. The variation in the spatial distribution of sleeping sites across the forest indicates that spider monkeys likely create a complex seed deposition pattern in space and time. However, the use of a very few tree species for sleeping could contribute to the establishment of specific vegetation associations typical of the southeastern Mexican rainforest, such as Terminalia-Dialium, and Brosimum-Dialium.     

Male and female range use in a group of white‐bellied spider monkeys (Ateles belzebuth) in Yasuní National Park,Ecuador

Spider monkeys (Ateles sp.) live in a flexible fission–fusion social system in which members of a social group are not in constant association, but instead form smaller subgroups of varying size and composition. Patterns of range use in spider monkeys have been described as sex‐segregated, with males and females often ranging separately, females utilizing core areas that encompass only a fraction of the entire community range, and males using much larger portions of the community range that overlap considerably with the core areas of females and other males. Males are also reported to use the boundary areas of community home ranges more often than females. Spider monkeys thus seem to parallel the “male‐bonded” patterns of ranging and association found among some groups of chimpanzees. Over several years of research on one group of spider monkeys (Ateles belzebuth) in Yasuní National Park, Ecuador, we characterized the ranging patterns of adult males and females and evaluated the extent to which they conform to previously reported patterns. In contrast to ranging patterns seen at several other spider monkey sites, the ranges of our study females overlapped considerably, with little evidence of exclusive use of particular areas by individual monkeys. Average male and female home range size was comparable, and males and females were similar in their use of boundary areas. These ranging patterns are similar to those of “bisexually bonded” groups of chimpanzees in West Africa. We suggest that the less sex‐segregated ranging patterns seen in this particular group of spider monkeys may be owing to a history of human disturbance in the area and to lower genetic relatedness between males, highlighting the potential for flexibility some aspects of the spider monkeys' fission–fusion social system. Am. J. Primatol. 72:129–141, 2010. © 2009 Wiley‐Liss, Inc.     

Structure of Brazilian Atlantic forests with occurrence of the woolly spider monkey (<Emphasis Type="Italic">Brachyteles hypoxanthus</Emphasis>)

This work examines patches of Atlantic forests in Minas Gerais State where woolly spider monkeys (Brachyteles hypoxanthus) are inhabitants in order to understand the effects of forest structure, diversity, and succession in B. hypoxanthus abundance. This study was carried out in three reserves: Rio Doce State Park (PERD), Mata do Sossego (Sossego), and Serra do Brigadeiro State Park (PESB). Structural studies were carried out by means of point-centered quarter samples in areas used by woolly spider monkeys. Evenness was lower in PERD than in the other two communities. By means of successional functional groups analysis and diametric structure, the PERD forest sample was shown to be in the later, and PESB forest sample in the earlier, stages of secondary succession. We found that tree species evenness and structural traits driven by succession were important factors in determining spider monkey abundance patterns. The PERD forest sample had lower evenness and had lower density of woolly spider monkeys than the Sossego forest sample. The lowest density of these primates was in the PESB forest sample, the earlier successional stage of secondary succession of this study.     

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.     

Sexual coercion does not exclude luring behavior in the climbing camel-spider <Emphasis Type="Italic">Oltacola chacoensis</Emphasis> (Arachnida,Solifugae, Ammotrechidae)

Sexual coercion in the form of forced copulation has been used as a typical example to illustrate the conflict of interests between females and males. Among arthropods, forced copulation has been reported for some groups of insects and crustaceans, but not for arachnids. In the present work, we analyse and describe the behavioral patterns of mating behavior of the climbing camel-spider, Oltacola chacoensis, relating it to relevant morphological features, In this species, the male forcefully clasps the female’s genital region with his chelicerae and locks her fourth pair of legs with his pedipalps. In some cases, the cuticle of the female’s abdomen was damaged by this cheliceral clasping. In contrast to other camel-spiders, the female O. chacoensis never remained motionless during mating, but continuously shook her body, opening her chelicerae notably towards the male. Despite this coercive context, males performed copulatory courtship (tapping with pedipalps) and females showed an apparent cooperative behavior (they remained still during a short period of the sperm transfer phase). These results strengthen the idea that sexual coercion (in the form of forced copulation) and luring behavior (in the form of copulatory courtship) are not two mutually-exclusive male’s strategies during a single copulation.     

Diet and Travel Costs for Spider Monkeys in a Nonseasonal, Hyperdiverse Environment

I studied the effects of a nonseasonal environment with a high diversity of plant species in a community of white-bellied spider monkeys (Ateles belzebuth belzebuth) in the Yasuní National Park, Ecuador. During 10 2-wk follows of focal individuals across 1 yr, I collected 1268 h of observation data on ranging and foraging. The environment had strong effects on both the foraging and ranging behavior of the monkeys. Yasuní spider monkeys are similar to spider monkeys in more seasonal environments in that ripe-fruit consumption dominates the diet. However, Yasuní spider monkeys exhibit an extremely diverse diet that parallels the variety of foods available to them, consuming more than 238 species of fruits. The impressive dietary variety increased even more with increased observation time, as I had not previously observed in the spider monkeys’ diet 40% of the fruit species the subjects consumed during the final follow. Ripe fruits remain the most important item in the diet year-round, supplemented with decayed wood or leaf flush. Local rarity of plant species means that fruiting patches are an average of 420 m apart, and mean patch residence times are short, only 8.1 min. Visits to an average of 11.5 feeding patches/d lead to a mean daily path length of 3311 m, longer than reported for any other Ateles species, and long compared to most other primate species. The long daily paths of Yasuní spider monkeys reflect travel costs resulting from foraging in a hyperdiverse nonseasonal environment.     

Olfactory Sensitivity for Six Predator Odorants in CD-1 Mice,Human Subjects,and Spider Monkeys

Using a conditioning paradigm, we assessed the olfactory sensitivity of six CD-1 mice (Mus musculus) for six sulfur-containing odorants known to be components of the odors of natural predators of the mouse. With all six odorants, the mice discriminated concentrations <0.1 ppm (parts per million) from the solvent, and with five of the six odorants the best-scoring animals were even able to detect concentrations <1 ppt (parts per trillion). Four female spider monkeys (Ateles geoffroyi) and twelve human subjects (Homo sapiens) tested in parallel were found to detect the same six odorants at concentrations <0.01 ppm, and with four of the six odorants the best-scoring animals and subjects even detected concentrations <10 ppt. With all three species, the threshold values obtained here are generally lower than (or in the lower range of) those reported for other chemical classes tested previously, suggesting that sulfur-containing odorants may play a special role in olfaction. Across-species comparisons showed that the mice were significantly more sensitive than the human subjects and the spider monkeys with four of the six predator odorants. However, the human subjects were significantly more sensitive than the mice with the remaining two odorants. Human subjects and spider monkeys significantly differed in their sensitivity with only two of the six odorants. These comparisons lend further support to the notion that the number of functional olfactory receptor genes or the relative or absolute size of the olfactory bulbs are poor predictors of a species’ olfactory sensitivity. Analysis of odor structure–activity relationships showed that in both mice and human subjects the type of alkyl rest attached to a thietane and the type of oxygen moiety attached to a thiol significantly affected olfactory sensitivity.