Development and mother-infant relations among captive patas monkeys

Generalizations about the rate of behavioral development and mother-infant relations in nonhuman primates are often based largely on observations of a few closely related species of macaques. Patas monkeys (Erythrocebus patas)are sufficiently distant phylogenetically and distinct in their social and ecological adaptations from the well-studied macaque species that observations of their patterns of infant development and mother-infant relations may indicate to what extent macaque patterns are typical of Old World monkey species. Eight patas infants living with their mothers in an established captive group were observed for 960 hr over the first year of life. These infants showed a rapid rate of behavioral development and attainment of independence from mothers. Patas also have one of the fastest rates of sexual maturation of any Old World monkey species. This pattern of rapid social and sexual development can be viewed as a response to a highly seasonal savannah environment in which there is a premium on ability to achieve nutritional, locomotor, and social self-sufficiency as quickly as possible and to reproduce as early and as often as developmental constraints will permit. Patterns of infant development and mother-infant relations may be best understood as an integral part of a species’ overall life history pattern.     

The ontogeny of sex differences in the behavior of patas monkeys

Many studies of sex differences in primates have been based on small experimental groups of peers in which only a limited range of social behavior could be expressed. In addition, the first few months of life are often the focus of such studies, with relatively little attention paid to older juveniles. In this study, 11 male and 9 female juvenile patas monkeys, living in a captive social group with all age-sex classes available, were observed between 1 and 4 years of age. A subset of seven patas monkeys was also observed between birth and 1 year of age. Here, we report the development of sex differences in independence, play, grooming, positioning behavior, and aggression over the juvenile period. Juvenile male patas monkeys played more and in longer bouts than females, but wrestling (rough-and-tumble play) was not more common among males. There were few differences in behaviors directed to male and female juveniles by other group members. Distinct differences emerged only in the behaviors of the juveniles themselves, with females being more active participants in social and aggressive interactions than males. In general, sex differences in patas monkeys show a mixture of patterns, some of which are predictive of adult sex differences and some of which appear to be specific to the particular demands of the juvenile period in this species     

Allomaternal behavior in a group of free-ranging patas monkeys

A free-ranging group of patas monkeys (Erythrocebus patas) containing 18 individually identifiable adult females was observed for approximately 400 hours, equally distributed over two two-month periods corresponding to the breeding and birth seasons, at the La Parguera facility of the Caribbean Primate Research Center. The large number of infants born in the spring and early summer (n = 14) allowed for detailed observations of alloparental behaviors, with a focus on allomothering by the adult females. Seven types of alloparental behaviors were recorded: contact, nuzzling, grooming, agonism, close visual inspection, attempted kidnapping, and kidnapping. Adult females emitted the vast majority of allomaternal behavior, the patterning and frequency of which closely resembled the patterning and frequency of inter-adult female social grooming. Relative dominance status of the participants did not consistently predict the directionality of allomothering. The most commonly observed allomaternal behaviors were contact and nuzzling, which are primarily affiliative behaviors; agonism was rare. Successful kidnapping occurred eight times. Immature monkeys (n = 22) emitted an additional 32 alloparental acts. A propensity towards allomothering by experienced females would be most beneficial to patas infants due to the patas' tendency towards dispersed foraging and rapid flight in the presence of danger. It is possible that direct competition with groups of rhesus macaques for available resources on the island served as a proximal cause for the allomothering observed in this patas group.     

Longitudinal study of dominance relations among captive patas monkeys

Eight and a half years of dominance relations within a captive group of patas monkeys were analyzed. It was found that matrilineal kinship significantly influenced individuals' ranks. In contrast, with the exception of certain intramatriline changes, increasing age had no predictable effect on overall rank, at least for females (this was untestable for males). Offspring typically challenged maternal dominance and in eight of twelve dyads, offspring either rose fully over their mothers (three cases, all daughters) or at least achieved dominance ambiguity with them. Additionally, two of the four younger sisters with an opportunity to rise in rank over an older sister did so. The group dominance hierarchy was unstable for 75% of the study due to a combination of agonistically induced and demographically induced rank changes. Concentration of the highest ranks in a single matriline showed a stronger association with group hierarchy stability than did the presence of an adult, nonnatal male. Group hierarchy stability was associated with increased affiliation (sitting close and sitting touching), but otherwise there were no behavioral correlations. Individuals' ranks within the group hierarchy were unrelated to their chances of being wounded or having diarrhea. Adult females' ranks were over twice as stable as the group hierarchy (57.1% stability), but stability/instability was not correlated with any behavioral changes. Available evidence suggests that dominance relations play only a minor role in the organization of patas monkeys' intragroup behavior. Am. J. Primatol. 42:41–51, 1997. © 1997 Wiley-Liss, Inc.     

Initiation of feeding by provisioned patas monkeys: Evidence for the protection hypothesis

The applicability of the baboon-based protection hypothesis was tested with data from a provisioned, free-ranging group of Erythrocebus patas.The age/sex class of the individual which first approached and fed from one of the food hoppers during early morning feeding sessions was noted for 114 mornings. The presence of an observer, and periodically, rhesus monkeys,near the hopper made these approaches analogous to progressions described for feral baboons. Adult patas of both sexes approached and ate first significantly more frequently than was expected based on their respective proportions in the group, and immature monkeys less often. For adult females,initiating feeding was not correlated with dominance rank, although females in the middle and lower thirds of the hierarchy (n = 6 in each third) initiated feeding more frequently than did the females in the top third. The protection hypothesis accounts for the observed behavioral pattern, while explanations based on competitive exclusion and dominance relationships do not adequately account for the results.     

Distribution and abundance of patas monkeys (Erythrocebus patas) in Laikipia, Kenya, 1979-2004

Patas monkeys may be especially vulnerable to local extinction because they live in relatively small, female-philopatric groups at low densities and are strongly polygynous. We assessed a patas monkey population in Kenya's 9,700 km(2) Laikipia District over 25 years, using data collected in 1979-1981 and 1992-2004. The data were based on intensive observations of three study groups, "on the ground" counts, and surveys of Laikipia residents. In 1979-1981, a minimum of 415 patas monkeys lived in 14-15 groups. By 2000, the best estimate suggested 310-445 patas monkeys living in 13-17 groups over a greater surveyed area, suggesting that patas monkeys in Laikipia may have undergone a slight decline in numbers over time. Their distribution, however, was similar over time. The relative stability of this population has likely been the result of beneficial co-existence with large-scale cattle ranching. Outside Laikipia, substantial habitat alteration from rising human populations has coincided with the near disappearance of patas monkeys where they were previously more numerous. The small population in Laikipia, probably the largest remaining in Kenya, may therefore be critical to the continued existence of patas monkeys in that country and may be dependent on maintenance of large-scale ranches. Such land use provides patas monkeys with water and broad expanses of Acacia drepanolobium woodlands, the habitat to which patas are restricted in Laikipia.     

Distribution of affiliative behaviors among adult females within a group of wild patas monkeys in a nonmating,nonbirth season

The distribution of four affiliative behaviors (proximity within 3 m, allogrooming, contact calling, and co-night-resting) were examined in a group of wild patas monkeys (Erythrocebus patas) during a nonmating, nonbirth season. To a greater or lesser extent, dominance rank and kinship influenced these behaviors of the adult females. Since high-ranking females tended to exhibit some of these behaviors with high frequency, they were considered to be acting as the focus of affiliative behaviors and as the center for group cohesion. Furthermore, related adult females also tended to exhibit some of these behaviors with a high frequency toward one another, so that matrilineal kinship was also seen to be an important factor for group cohesion. In contrast, the harem male tended to exhibit these behaviors at a low frequency and/or had no affiliative partner for any of them. Thus, it appears that the social organization of the patas group is concentric, being composed of high-ranking females in the center, low-ranking females at the periphery, and the harem male at the distant periphery.     

Patterns of mating among male patas monkeys (Erythrocebus patas) in Kenya

An habituated group of wild patas monkeys was observed in Kenya for 550 h in 1984. Observations were made primarily during an interval that, as previous studies at the same site had demonstrated, coincided with the annual mating and conception periods. Earlier field studies of patas at other sites had reported that heterosexual patas groups had only a single resident adult male and that mating was harem-polygynous. At the Kenya site, by contrast, as many as six males were simultaneously resident and mated in the group during the conception period. Males adopted a variety of tactics to gain access to receptive females, ranging from opportunistic mating to attempts at sequestration that resembled consort behavior in other cercopithecoids such as savanna baboons and rhesus macaques. Aggressive competition for access to females took place among the males, although the number of completed copulations per male did not bear a positive relation to agonistic dominance rank. For patas monkeys, harem polygyny is only one available option within an overall mating system that is best described as a form of promiscuous polygyny, especially during periods when conception is most likely.     

Social and environmental determinants of reproductive cycles in patas monkeys

The menstrual cycles of a captive group of patas monkeys were followed for 15 months by taking vaginal smears and lavages three times a week. Without an adult male in the group, menstrual cycles still showed the expected qualitative changes previously associated with the onset and with the end of a mating period. The addition of an adult male to the female group, once mating season cycles were evident, did not result in further changes in erythrocytes or sediment levels in vaginal samples or cycle regularity. Menstrual-cycle onsets for related females were significantly more synchronized than onsets for unrelated females. Preliminary observations on adult male patas housed separately from the females indicate that they too undergo seasonal changes in physiology and behavior.     

Diet for a small primate: Insectivory and gummivory in the (large) patas monkey (Erythrocebus patas pyrrhonotus)

A 17 month field study of unprovisioned patas monkeys (Erythrocebus patas pyrrhonotus) in Laikipia, Kenya, using both ad libitum and scan sampling techniques, revealed that the diet of patas monkeys consists primarily of gum of Acacia drepanolobium, arthropods (both free-living and concentrated in the swollen thorns of A. Drepanolobium), and other animals. This type of diet is normally found only in smaller-bodied primates. Results from vegetational transects suggest that the larger-bodied patas monkey can subsist on such a diet because gum and arthropods are relatively easily found in their habitat, thereby minimizing search time. Patas monkeys also spend more time moving and less time feeding (while not moving) than other Old World primates. The characteristic long limbs of patas may have evolved in response to feeding on small, nonusurpable, and widely distributed foods, in which access to foods is maximized while time and energy spent in terrestrial travel between food sites are minimized. Am. J. Primatol. 45:381–398, 1998. © 1998 Wiley-Liss, Inc.     

Comparison of responses to alarm calls by patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure

We studied responses to alarm calls of sympatric patas (Erythrocebus patas) and vervet (Cercopithecus aethiops) monkeys in relation to habitat structure, with the intention of understanding the relationship between the environment and predator avoidance. Patas and vervet monkeys are phylogenetically closely related and overlap in body size. However, while patas monkeys are restricted to nonriverine habitats at our study site, vervets use both nonriverine and riverine habitats, allowing us to "vary" habitat structure while controlling for effects of group size, composition, and phylogeny. Patas monkeys in the nonriverine habitat responded to mammalian predator alarm calls with a greater variety of responses than did vervets in the riverine habitat, but not when compared with vervets in the nonriverine habitat. Ecological measurements confirm subjective assessments that trees in the riverine habitat are significantly taller and occur at lower densities than trees in the nonriverine habitat. Despite the lower density of trees in the riverine habitat, locomotor behavior of focal animals indicates that canopy cover is significantly greater in the riverine than the nonriverine habitat. Differences in responses to alarm calls by the same groups of vervets in different habitat types, and convergence of vervets with patas in the same habitat type, suggest that habitat type can be a significant source of variation in antipredator behavior of primates.     

Infant-directed behavior in young rhesus monkeys: Sex differences and effects of prenatal androgens

Young (3–4 years old) laboratory-reared rhesus monkeys were observed in five 15-minute tests with 1–15-day-old infants. Males and females were equally likely to investigate infants. Females communicated more with infants by grin-lipsmacking and gurgling–-gestures that were not shown by any males. More females presented the ventrum to infants than did males. Females contacted infants more than did males by grooming, crouching over, and having full body contact with them. To see whether prenatal androgens produced the male pattern of response, we conducted similar tests with pseudohermaphrodites (prenatally androgenized genetic females) and neonatally castrated males. On most sexually dimorphic behaviors, pseudohermaphrodites behaved more like females than like males. Castrated males, like females and pseudohermaphrodites, crouched over infants more than did intact males. Castrated males differed from females only on one infant-directed response, the grin-lipsmack. These comparisons showed that defeminization of the repertoire of infant-directed responses was measurable only in intact males. We conclude accordingly that prenatal androgens alone are not responsible for defeminization of this repertoire and that a contribution from postnatal androgens is likely to be necessary.     

Ecological determinants of the behavior and social structure of Japanese monkeys: A synthesis

A review is presented of the results of the various studies in this volume and an attempt is made to establish connections among several features of the ecology, behavior, and social structure of Japanese monkeys. Several studies in this volume suggest that intergroup direct feeding competition has been much more severe in Yakushima, in the warm-temperate region, than in Kinkazan, in the cool-temperate region of Japan. This result is consistent with the predictions that moderate abundance and clumped distribution of food incur more severe intergroup direct competition. However, the number of adult females within a group in Yakushima was smaller than that in Kinkazan even though severe intergroup direct competition should favor large groups. This contradiction can be mainly explained by the less severe intergroup indirect competition in Kinkazan than in Yakushima. By contrast, some studies in this volume also indicate that adult male to female ratio within a group has been higher in Yakushima than in Kinkazan. This result can be explained in two ways: the females in Yakushima might have recruited more males to increase the competitive ability of the group under conditions of severe intergroup direct feeding competition; alternatively, it might be profitable that the males in Yakushima defend females cooperatively as group males against the males in other groups at a moderate density of females. Some studies in this volume suggest that grooming frequency was higher in Yakushima than in Kinkazan. The higher grooming frequency in Yakushima might have been partly due to a constant increase in engaging in social behavior from a decrease in feeding time. Another reason might be that there is a stronger effect of grooming on promotion of formation of coalitions among adults under conditions of severe intergroup direct and intragroup direct competition.     

莲藕食根金花虫成虫活动行为的日节律

【目的】通过莲藕食根金花虫Donacia provostii Fairmaire成虫日活动行为节律的系统研究,以期为构建该虫的高效防控技术体系提供科学依据。【方法】采用室外单头隔离和雌雄配对饲养,将莲藕食根金花虫成虫的行为划分为离水静息、触水静息、取食、移动、交配和产卵6个类型,每30 min观察记录一次其活动行为,连续5 d,统计分析其活动行为的日节律。【结果】在时间上,莲藕食根金花虫成虫各行为在各时间点间和时间段间均存在极显著差异(P<0.001);在空间上,成虫各行为在不同位置发生的比例存在极显著差异(P<0.001)、且荇菜叶上和水面的各行为在不同时间点间存在极显著差异(P<0.001)。【结论】莲藕食根金花虫成虫活动行为存在时空上的差异,空间对其行为的影响较时间明显。     

稻水象甲成虫活动行为的日节律

为了摸清稻水象甲Lissorhoptrus oryzophilus Kuschel成虫在稻田中的日活动行为节律, 采用室外单头隔离饲养的方法, 将成虫 行为分为移动、 取食、 离水静息、 触水静息和其他5个行为类型, 每30 min观察记录1次, 从2012年4月30日至5月4日连续观察5 d, 共获得7 200个行为数据。结果显示： 稻水象甲越冬成虫行为的日时间分配以离水静息行为最多（47.83%）, 移动行为最少（5.64%）, 各行为的时间分配存在极显著差异（P<0.001）。离水静息行为最高峰值在23:30 （72.67%）, 最低值在7:30 （14.67%）; 触水静息行 为最大峰值在7:30 （75.33%）, 19:00还有一个小高峰（37.33%）; 取食行为在15:00达到最高峰（26.67%）, 在21:00达到第2个高峰 值（18.00%）; 移动行为在22:00-9:00较少（0~4.00%）, 从9:30开始持续增加, 在17:00达到最高峰（20.00%）; 其他行为在 1.33~18.67%之间波动。离水静息、 移动、 取食和其他行为白天和黑夜存在极显著差异（P<0.001）, 但触水静息行为白天和黑夜无显著 不同（P=0.834）; 上午、 中午、 下午和晚上4个时间段之间各行为也有显著差异（P<0.001）。在空间上, 离水静息行为在叶片上最高 , 移动行为以水中最高, 取食行为仅发生在叶片上, 离水静息、 移动和取食在水稻不同部位存在极显著差异（P<0.001）。水中发生触 水静息、 移动和其他共3种行为, 以触水静息行为的日波动最大, 3种行为在各时刻之间有极显著差异（触水静息和移动： P<0.001; 其他： P=0.002）; 叶片上发生离水静息、 移动和取食3种行为, 以离水静息和取食行为的日波动较大且在各时刻间具有极显著的差异 （P<0.001）; 茎秆和瓶壁或封口纱布处主要发生离水静息和移动行为, 所占比例均不高, 但在瓶壁或封口纱布处的移动行为各时刻之 间有极显著差异（P=0.008）。水中和叶片上是行为发生的主要空间, 在水中行为的最高峰值（81.33%）与叶片上的最低值（12.00%）出 现时间相同, 为7:30, 一天中各时刻水中和叶片上的行为呈交错性变化。结果提示, 稻水象甲成虫活动行为受到时空变化的影响, 且 时间变化对其行为的影响较空间变化更为明显。     

粪食性金龟的行为及其适应演化

粪食性金龟的行为简单分为3类:粪居型(endocoprid或dwelling behaviour)、直接掘洞型(paracoprid或tunnelling behaviour)和滚粪球型(telocoprid或rolling behaviour)。文章详细阐述各类型的特点,探讨粪食性金龟行为的进化趋势和过程,并进一步阐述粪食性金龟的适应演化。     

Diurnal changes of behavior and respiration of Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) in captivity

A preliminary study was carried out to investigate diurnal changes of behavior of three, one adult male, one adult female, and one juvenile female, Yangtze finless porpoises (Neophocaena phocaenoides asiaeorientalis) in captivity. The respiration and behavior of the porpoises were recorded for 222 hr across 42 days. Behavioral data were recorded for eight general categories: aerial display and fast swimming, begging for fish, playing, nonsexual socializing, sexual behavior, resting, rubbing, and miscellaneous (i.e., other behaviors not included in the above categories). Each behavioral category was scored using one‐zero sampling with 10‐min intervals. The adult male showed shorter mean respiratory intervals at night (19:00–7:00 h), whereas the mean respiratory intervals of the females were shorter during the day (7:00–19:00 h). Begging for fish of all individuals, playing of the juvenile female, nonsexual socializing, and miscellaneous behavior of the adult female and resting of the male were observed more easily in the day, and aerial display and fast swimming of the adults and resting of the females were observed more easily at night. No significant diurnal difference was found, however, in the remaining categories of each individual. Each of the three porpoises therefore showed a distinct diurnal pattern, but none was obviously more active in the daytime than during the nighttime. Results suggest that daytime‐only feeding schedules may be insufficient to meet the energetic needs of marine mammals that show a 24‐hr activity cycle, and that nighttime feeding may be a worthwhile addition to husbandry routines. Zoo Biol 0:1–11, 2005. © 2005 Wiley‐Liss, Inc.     

Effects of corticotropin-releasing factor (CRF), tuftsin and dermorphin on behavior of squirrel monkeys maintained by different events

The effects of intracerebroventricular (ICV) administration of ovine CRF (0.1–30.0 μg/kg), dermorphin (0.3–30.0 μg/kg) and tuftsin (10–3000 μg/kg) were examined in squirrel monkeys trained to respond under a multiple 3-min fixed-interval schedule of food presentation and either shock presentation or stimulus-shock termination. Initial administration of the 41-amino acid polypeptide CRF increased food-maintained responding by 150–200% in 2 of 3 subjects. However, no other doses tested affected response rates, a result that may have been due to the rapid development of tolerance. The tetrapeptide tuftsin selectively increased responding maintained by food presentation at doses that decreased shock-maintained responding. The heptapeptide dermorphin selectively increased food-maintained responding when responding in the other component of the multiple schedule was maintained by shock presentation. When responding was maintained by a multiple food, stimulus-shock termination schedule, dermorphin decreased response rates in both components. Dermorphin's rate increases were blocked by the opiate antagonist naloxone, indicating that dermorphin's actions were mediated through the opiate receptor. These results indicate that the behavioral effects of tuftsin, dermorphin, and perhaps CRF, depend on the manner in which responding is controlled by its consequences. While the actions of tuftsin and dermorphin are believed to be mediated through the opiate system, the behavioral effects observed in primates appear different from the effects of morphine under similar schedule conditions.     

How laboratory-raised Japanese monkeys (Macaca fuscata) perceive rotated photographs of monkeys: Evidence for an inversion effect in face perception

Five laboratory-raised Japanese monkeys (Macaca fuscata) were presented various types of photographs of Japanese and rhesus monkeys (Macaca mulatta) in upright, horizontal, and inverted orientations in a sensory-reinforcement experiment. The ratio of the duration of potential viewing time for the photographs which the subjects controlled to the interval between subject-controlled presentations of them (the D/I score) was used as a measure of preference for the photographs. When inverted photographs were presented, the D/I scores were lower than for upright photographs. The difference in D/I scores between photographs of the two species, which indicated discriminability between them, also diminished when the photographs were inverted. The results obtained suggest an inversion effect in face perception in macaque monkeys.     

First evidence of prey capture and meat eating by wild Yunnan snub-nosed monkeys Rhinopithecus bieti in Yunnan,China

Most extant nonhuman primates occasionally prey on fast-moving, warm-blooded animals; however, Indriidae, Lepilemuridae, and Colobinae either scavenged for meat or did not eat meat at all. Here we report six cases of animal consumption by the snub-nosed monkey Rhinopithecus bieti in a wild, habituated group between 2004 and 2009 in Yunnun, China. At present,only males in an all-male unit within the study group were involved in active hunting. Such a male-biased activity may be related to the group structure and spatial spread of R. bieti. Two females were observed eating freshly killed birds. The findings confirmed that R. bieti engaged in scavenging and, when hunting, employed a cranio-cervical bite to kill their prey. Meat eating is likely a nutrient maximization feeding strategy in R. bieti, especially in males. A begging behavior occurred after successful prey capture. Although begging was observed, no sharing of the meat was seen. The present findings illuminate the dietary diversity of R. bieti and their ability to expand their dietary spectrum.